Intrinsic muscle clock is necessary for musculoskeletal health
Open accessAbstract
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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Disruption of the muscle clock has significant impact on glucose intolerance and insulin resistance with very small changes in fiber types.
“Disruption of the muscle clock has also been shown to have significant impact on glucose intolerance and insulin resistance with very small changes in fiber types (Dyar et al., 2014; Schroder et al., 2015; Harfmann et al., 2016).”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Schroder et al., 2015
Prolonged loss of Bmal1 function is associated with increased fibrosis within muscle.
“In addition, prolonged loss of Bmal1 function was also associated with increased fibrosis within the muscle.”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Schroder et al., 2015
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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
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
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 · see citing works
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 · see citing works
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 · see citing works
Hughes, M. E., Hogenesch, J. B., & Kornacker, K. (2010) · Journal of Biological Rhythms · doi:10.1177/0748730410379711 · Cited by 1,087 · see citing works
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 · see citing works
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× · see citing works
“Physiological cross-sectional area was estimated according to Brooks & Faulkner (1988) and used to calculate specific force.”
MethodRajaratnam, S. M., & Arendt, J. (2001) · The Lancet · doi:10.1016/s0140-6736(01)06108-6 · Cited by 711 · see citing works
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 626 · see citing works
Effective fiber hypertrophy in satellite cell-depleted skeletal muscle
McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., Srikuea, R., Lawson, B. A., Grimes, B., Keller, C., et al. (2011) · Development · doi:10.1242/dev.068858 · Cited by 616 · see citing works
Self-citationMolecular Genetics of Circadian Rhythms in Mammals
King, D. P., & Takahashi, J. S. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.713 · Cited by 551 · 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
The effect of ageing and immobilization on structure and function of human skeletal muscle fibres
D’Antona, G. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.046276 · Cited by 477 · see citing works
Obesity in mice with adipocyte-specific deletion of clock component Arntl
Paschos, G. K., Ibrahim, S., Song, W.-L., Kunieda, T., Grant, G., Reyes, T. M., Bradfield, C. A., Vaughan, C. H., Eiden, M., Masoodi, M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2979 · Cited by 465 · see citing works
Skeletal muscle weakness in old age: underlying mechanisms.
Brooks, S. V., & Faulkner, J. A. (1994) · PubMed · Cited by 463 · see citing works
Storch, K.-F., Paz, C., Signorovitch, J., Raviola, E., Pawlyk, B., Li, T., & Weitz, C. J. (2007) · Cell · doi:10.1016/j.cell.2007.06.045 · Cited by 460 · 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
Fry, C. S., Lee, J. D., Mula, J., Kirby, T. J., Jackson, J. R., Liu, F., Yang, L., Mendias, C. L., Dupont-Versteegden, E. E., McCarthy, J. J., et al. (2015) · Nature Medicine · doi:10.1038/nm.3710 · Cited by 432 · see citing works
von Maltzahn, J., Chang, N. C., Bentzinger, C. F., & Rudnicki, M. A. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.07.008 · Cited by 393 · see citing works
Andrews, J. L., Zhang, X., McCarthy, J. J., McDearmon, E. L., Hornberger, T. A., Russell, B., Campbell, K. S., Arbogast, S., Reid, M. B., Walker, J. R., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014523107 · Cited by 389 · cited 7× · see citing works
“Our previous work has demonstrated that muscle force per unit cross section (specific force) measured in vitro is significantly reduced in the EDL muscles/muscle fibres of the 12- to 14-week-old Bmal1 KO mouse compared to wild-type controls (Andrews et al. 2010).”
BackgroundMethodInfluentialSelf-citationDeterminants of Muscle and Bone Aging
Curtis, E., Litwic, A., Cooper, C., & Dennison, E. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25001 · Cited by 375 · see citing works
CircaDB: a database of mammalian circadian gene expression profiles
Pizarro, A., Hayer, K. E., Lahens, N. F., & Hogenesch, J. B. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1161 · Cited by 367 · see citing works
Skeletal muscle weakness in old age
Brooks, S. V., & Faulkner, J. A. (1994) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199404000-00006 · Cited by 364 · 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
Dissecting the Functions of the Mammalian Clock Protein BMAL1 by Tissue-Specific Rescue in Mice
McDearmon, E. L., Patel, K., Ko, C. H., Walisser, J. A., Schook, A. C., Chong, J. L., Wilsbacher, L. D., Song, E. J., Hong, H., Bradfield, C. A., et al. (2006) · Science · doi:10.1126/science.1132430 · Cited by 321 · see citing works
Aging of skeletal muscle fibers
Miljkovic, N., Lim, J.-Y., Miljkovic, I., & Frontera, W. R. (2015) · Annals of Rehabilitation Medicine · doi:10.5535/arm.2015.39.2.155 · Cited by 309 · cited 1× · see citing works
“A well-known feature of ageing in skeletal muscle is a shift in fibre type characterized by a decrease in the type IIB fibres with increases in the more oxidative type IIA fibres (Ciciliot et al. 2013; Miller et al. 2014; Purves-Smith et al. 2014; Miljkovic et al. 2015).”
BackgroundNeural control of aging skeletal muscle
Delbono, O. (2003) · Aging Cell · doi:10.1046/j.1474-9728.2003.00011.x · Cited by 248 · see citing works
Interactions Between Muscle Tissues and Bone Metabolism
Kawao, N., & Kaji, H. (2014) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25040 · Cited by 231 · see citing works
The impact of sleep on age-related sarcopenia: Possible connections and clinical implications
Piovezan, R. D., Abucham, J., dos Santos, R. V. T., de Mello, M. T., Tufik, S., & Poyares, D. R. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.003 · Cited by 215 · see citing works
Antagonists of Wnt and BMP signaling promote the formation of vertebrate head musclePreprint
Tzahor, E., Kempf, H., Mootoosamy, R. C., Poon, A. C., Abzhanov, A., Tabin, C. J., Dietrich, S., & Lassar, A. B. (2003) · Genes & Development · doi:10.1101/gad.1154103 · Cited by 215 · see citing works
Progressive arthropathy in mice with a targeted disruption of theMop3/Bmal-1 locus
Bunger, M. K., Walisser, J. A., Sullivan, R., Manley, P. A., Moran, S. M., Kalscheur, V. L., Colman, R. J., & Bradfield, C. A. (2005) · genesis · doi:10.1002/gene.20102 · Cited by 207 · see citing works
Changes in triceps surae muscle architecture with sarcopenia
Morse, C. I., Thom, J. M., Birch, K. M., & Narici, M. V. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01404.x · Cited by 206 · see citing works
Myostatin (GDF-8) as a key factor linking muscle mass and bone structure.
Elkasrawy, M., & Hamrick, M. W. (2010) · PubMed · Cited by 203 · 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
Andrews, Z. B., Horvath, B., Barnstable, C. J., Elseworth, J., Yang, L., Beal, M. F., Roth, R. H., Matthews, R. T., & Horvath, T. L. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4269-04.2005 · Cited by 199 · see citing works
Lying low but ready for action: the quiescent muscle satellite cell
Montarras, D., L’honoré, A., & BUCKINGHAM, M. E. (2013) · FEBS Journal · doi:10.1111/febs.12372 · Cited by 199 · see citing works
Inducible Cre transgenic mouse strain for skeletal muscle-specific gene targeting
McCarthy, J. J., Srikuea, R., Kirby, T. J., Peterson, C. A., & Esser, K. A. (2012) · Skeletal Muscle · doi:10.1186/2044-5040-2-8 · Cited by 194 · see citing works
The effect of aging on gait parameters in able-bodied older subjects: a literature review
Aboutorabi, A., Arazpour, M., Bahramizadeh, M., Hutchins, S. W., & Fadayevatan, R. (2015) · Aging Clinical and Experimental Research · doi:10.1007/s40520-015-0420-6 · Cited by 191 · see citing works
Skeletal muscle is an endocrine organ
Iizuka, K., Machida, T., & Hirafuji, M. (2014) · Journal of Pharmacological Sciences · doi:10.1254/jphs.14r02cp · Cited by 189 · see citing works
Chang, N. C., & Rudnicki, M. A. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00006-8 · Cited by 180 · see citing works
Hodge, B. A., Wen, Y., Riley, L. A., Zhang, X., England, J. H., Harfmann, B. D., Schroder, E. A., & Esser, K. A. (2015) · Skeletal Muscle · doi:10.1186/s13395-015-0039-5 · Cited by 175 · see citing works
Clock Genes and Clock-Controlled Genes in the Regulation of Metabolic Rhythms
Mazzoccoli, G., Pazienza, V., & Vinciguerra, M. (2012) · Chronobiology International · doi:10.3109/07420528.2012.658127 · Cited by 171 · see citing works
Development of dilated cardiomyopathy in<i>Bmal1</i>-deficient mice
Lefta, M., Campbell, K. S., Feng, H.-Z., Jin, J.-P., & Esser, K. A. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00238.2012 · Cited by 158 · see citing works
Self-citationQuiat, D., Voelker, K. A., Pei, J., Grishin, N. V., Grange, R. W., Bassel‐Duby, R., & Olson, E. N. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107413108 · Cited by 151 · see citing works
The cardiomyocyte molecular clock, regulation of <i>Scn5a</i> , and arrhythmia susceptibility
Schroder, E. A., Lefta, M., Zhang, X., Bartos, D. C., Feng, H.-Z., Zhao, Y., Patwardhan, A., Jin, J.-P., Esser, K. A., & Delisle, B. P. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00383.2012 · Cited by 147 · see citing works
Self-citationMultistage genome-wide association meta-analyses identified two new loci for bone mineral density
Zhang, L., Choi, H. J., Estrada, K., Leo, P. J., Li, J., Pei, Y., Zhang, Y., Lin, Y., Shen, H., Liu, Y.-Z., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt575 · Cited by 146 · see citing works
Antoch, M. P., Gorbacheva, V., Vykhovanets, O. V., Toshkov, I. A., Kondratov, R. V., Kondratova, A. A., Lee, C., & Nikitin, A. Y. (2008) · Cell Cycle · doi:10.4161/cc.7.9.5886 · Cited by 144 · see citing works
Cellular oscillators: rhythmic gene expression and metabolism
Schibler, U., & Naef, F. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.01.007 · Cited by 138 · see citing works
Yoshitane, H., Ozaki, H., Terajima, H., Du, N., Suzuki, Y., Fujimori, T., Kosaka, N., Shimba, S., Sugano, S., Takagi, T., et al. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01465-13 · Cited by 137 · see citing works
The search for exercise factors in humans
Catoire, M., & Kersten, S. (2015) · The FASEB Journal · doi:10.1096/fj.14-263699 · Cited by 137 · see citing works
Timing of circadian genes in mammalian tissues
Korenčič, A., Košir, R., Bordyugov, G., Lehmann, R., Rozman, D., & Herzel, H. (2014) · Scientific Reports · doi:10.1038/srep05782 · Cited by 117 · see citing works
The Clock Genes Period 2 and Cryptochrome 2 Differentially Balance Bone Formation
Maronde, E., Schilling, A. F., Seitz, S. A., Schinke, T., Schmutz, I., van der Horst, G. T. J., Amling, M., & Albrecht, U. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011527 · Cited by 117 · see citing works
Brain-Specific Rescue of Clock Reveals System-Driven Transcriptional Rhythms in Peripheral Tissue
Hughes, M. E., Hong, H., Chong, J. L., Indacochea, A. A., Lee, S. S., Han, M., Takahashi, J., & Hogenesch, J. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002835 · Cited by 116 · see citing works
Effects of myostatin deletion in aging mice
Morissette, M. R., Stricker, J., Rosenberg, M. A., Buranasombati, C., Levitan, E. B., Mittleman, M. A., & Rosenzweig, A. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00508.x · Cited by 116 · see citing works
The daily rhythms of genes, cells and organs
Schibler, U. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400424 · Cited by 116 · see citing works
Purves-Smith, F. M., Sgarioto, N., & Hepple, R. T. (2014) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000012 · Cited by 114 · see citing works
Matching of Calcineurin Activity to Upstream Effectors Is Critical for Skeletal Muscle Fiber Growth
Dunn, S. E., Chin, E. R., & Michel, R. N. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.663 · Cited by 113 · see citing works
Brain and Muscle Arnt-like 1 is a Key Regulator of Myogenesis
Chatterjee, S., Nam, D., Guo, B., Kim, J. M., Winnier, G. E., Lee, J., Berdeaux, R., Yechoor, V. K., & Ma, K. (2013) · Journal of Cell Science · doi:10.1242/jcs.120519 · Cited by 104 · see citing works
Circadian regulation of cell cycle: Molecular connections between aging and the circadian clock
Khapre, R. V., Samsa, W. E., & Kondratov, R. V. (2010) · Annals of Medicine · doi:10.3109/07853890.2010.499134 · Cited by 95 · see citing works
The effect of ageing and immobilization on structure and function of human skeletal muscle fibres
D’Antona, G., Pellegrino, M. A., Adami, R., Rossi, R., Carlizzi, C. N., Canepari, M., Saltin, B., & Bottinelli, R. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00499.x · Cited by 84 · see citing works
Miller, M. S., Callahan, D. M., & Toth, M. J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00369 · Cited by 79 · see citing works
Su, W., Xie, Z., Guo, Z., Duncan, M. J., Lutshumba, J., & Gong, M. C. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00825.2011 · Cited by 78 · see citing works
Richard, A.-F., Demignon, J., Sakakibara, I., Pujol, J., Favier, M., Strochlic, L., Grand, F. L., Sgarioto, N., Guernec, A., Schmitt, A., et al. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.010 · Cited by 70 · see citing works
Arounleut, P., Bialek, P., Liang, L.-F., Upadhyay, S. K., Fulzele, S., Johnson, M. H., Elsalanty, M. E., Isales, C. M., & Hamrick, M. W. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.06.004 · Cited by 66 · see citing works
Quantitative electrophoretic analysis of myosin heavy chains in single muscle fibers
Tikunov, B. A., Sweeney, H. L., & Rome, L. C. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.5.1927 · Cited by 65 · see citing works
Age- and Gender-Related Changes in Contractile Properties of Non-Atrophied EDL Muscle
Chan, S., & Head, S. I. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012345 · Cited by 63 · see citing works
Zhang, X., Patel, S. P., McCarthy, J. J., Rabchevsky, A. G., Goldhamer, D. J., & Esser, K. A. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1297 · Cited by 62 · see citing works
Isaac, C. E., Wright, A., Ūsas, A., Li, H., Tang, Y., Mu, X., Greco, N., Dong, Q. D., Vo, N. N., Kang, J. D., et al. (2012) · Journal of Orthopaedic Research® · doi:10.1002/jor.22236 · Cited by 61 · see citing works
Miyazaki, M., Schroder, E. A., Edelmann, S. E., Hughes, M. E., Kornacker, K., Balke, C. W., & Esser, K. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027168 · Cited by 58 · see citing works
Yablonka‐Reuveni, Z., & Rivera, A. J. (1997) · Growth Factors · doi:10.3109/08977199709002109 · Cited by 57 · see citing works
Skeletal Muscle Degeneration and Regeneration in Mice and Flies
Rai, M., Nongthomba, U., & Grounds, M. D. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-391498-9.00007-3 · Cited by 55 · see citing works
Atwood, A., DeConde, R. P., Wang, S. S., Mockler, T. C., Sabir, J. S. M., Ideker, T. E., & Kay, S. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115753108 · Cited by 45 · see citing works
Gait Speed and Dismobility in Older Adults
Ostir, G. V., Berges, I. M., Ottenbacher, K. J., Fisher, S. R., Barr, E. A., Hebel, J. R., & Guralnik, J. M. (2015) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2015.05.017 · Cited by 44 · see citing works
Scimè, A., Desrosiers, J., Trensz, F., Palidwor, G., Caron, A. Z., Andrade-Navarro, M. A., & Grenier, G. (2009) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2009.11.001 · Cited by 40 · see citing works
Khodabukus, A., & Baar, K. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24848 · Cited by 37 · see citing works
Biesiadecki, B. J., Schneider, K. L., Yu, Z.-B., Chong, S. M., & Jin, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314225200 · Cited by 34 · see citing works
Time and frequency domain analysis of acoustic signals from a human muscle
Chen, D.-M., Durand, L., & Bellemare, F. (1997) · Muscle and Nerve · doi:10.1002/(sici)1097-4598(199708)20:8 · Cited by 12 · see citing works
Wagers, A. J. (2008) · Cell stem cell · doi:10.1016/j.stem.2007.12.005 · Cited by 9 · see citing works
Wnt Proteins in Mineralized Tissue Development and Homeostasis
Tompkins, K. A. (2011) · Connective Tissue Research · doi:10.3109/03008207.2011.616610 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Harrison DE (2011). Life Span as a Biomarker. The Jackson Laboratory. Available at: https://www.jax.org/research‐and‐faculty/research‐labs/the‐harrison‐lab/gerontology/life‐span‐as‐a‐biomarker. [Google Scholar]
- Quinlan JG, Cambier D, Lyden S, Dalvi A, Upputuri RK, Gartside P, Michaels SE & Denman D (1997). Regeneration‐blocked mdx muscle: in vivo model for testing treatments. Muscle Nerve 20, 1016–1023. [DOI] [PubMed] [Google Scholar]
Cited by
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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
Muscle‐bone crosstalk and potential therapies for sarco‐osteoporosis
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Maurel, D. B., Jähn, K., & Lara-Castillo, N. (2017) · Biomedicines · doi:10.3390/biomedicines5040062 · Cited by 122 · see citing works
Effects of exercise on circadian rhythms in humans
Shen, B., Ma, C., Wu, G., Liu, H., Chen, L., & Yang, G. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1282357 · Cited by 125 · see citing works
Circadian Metabolism: From Mechanisms to Metabolomics and Medicine
Brown, S. A. (2016) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2016.03.015 · Cited by 118 · see citing works
Aoyama, S., & Shibata, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00063 · Cited by 106 · see citing works
Metabolism and exercise: the skeletal muscle clock takes centre stage
Martin, R. A., Viggars, M. R., & Esser, K. A. (2023) · Nature Reviews Endocrinology · doi:10.1038/s41574-023-00805-8 · Cited by 101 · see citing works
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
Regulation of Skeletal Homeostasis
Zaidi, M., Yuen, T., Sun, L., & Rosen, C. J. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00050 · Cited by 92 · see citing works
Molecular Connections Between Circadian Clocks and Aging
Welz, P.-S., & Benitah, S. A. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.036 · Cited by 87 · 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 Regulation of Adult Stem Cell Homeostasis and Aging.
Benitah, S., & Welz, P. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.05.002 · Cited by 80 · see citing works
Викторович, П. Д., Makhnovskii, P. A., Shagimardanova, E. I., Gazizova, G. R., Lysenko, E. A., Gusev, O., & Виноградова, О. Л. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00449.2018 · Cited by 80 · see citing works
Time of Day and Muscle Strength: A Circadian Output?
Douglas, C. M., Hesketh, S. J., & Esser, K. A. (2020) · Physiology · doi:10.1152/physiol.00030.2020 · Cited by 80 · see citing works
A role for circadian clock in metabolic disease
Shimizu, I., Yoshida, Y., & Minamino, T. (2016) · Hypertension Research · doi:10.1038/hr.2016.12 · Cited by 79 · see citing works
Circadian rhythms affect bone reconstruction by regulating bone energy metabolism
Luo, B., Zhou, X., Tang, Q., Yin, Y., Feng, G., Li, S., & Chen, L. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-03068-x · Cited by 69 · 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
Glucose Homeostasis: Regulation by Peripheral Circadian Clocks in Rodents and Humans
Gachon, F., Loizides‐Mangold, U., Petrenko, V., & Dibner, C. (2017) · Endocrinology · doi:10.1210/en.2017-00218 · Cited by 63 · see citing works
Circadian transcription from beta cell function to diabetes pathophysiology
Perelis, M., Ramsey, K. M., Marcheva, B., & Bass, J. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416656949 · Cited by 57 · see citing works
Circadian clock communication during homeostasis and ageing
Mortimer, T., Smith, J. G., Muñoz‐Cánoves, P., & Benitah, S. A. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00802-3 · Cited by 54 · 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
Intensity-dependent gene expression after aerobic exercise in endurance-trained skeletal muscle
Викторович, П. Д., Makhnovskii, P. A., Kurochkina, N. S., Lysenko, E. A., Vepkhvadze, T. F., & Виноградова, О. Л. (2018) · Biology of Sport · doi:10.5114/biolsport.2018.77828 · Cited by 45 · see citing works
Daytime-restricted feeding enhances running endurance without prior exercise in mice
Xin, H., Huang, R., Zhou, M., Chen, J., Zhang, J., Zhou, T., Ji, S., Liu, X., Tian, H., Lam, S. M., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00826-7 · Cited by 44 · see citing works
Hunt, L. C., Jiao, J., Wang, Y., Finkelstein, D., Rao, D., Curley, M., Robles‐Murguia, M., Shirinifard, A., Pagala, V., Peng, J., et al. (2019) · Genome Research · doi:10.1101/gr.246884.118 · Cited by 42 · see citing works
Bone circuitry and interorgan skeletal crosstalk
Zaidi, M., Kim, S.-M., Mathew, M., Korkmaz, F., Sultana, F., Miyashita, S., Gumerova, A. A., Frolinger, T., Moldavski, O., Barak, O., et al. (2023) · eLife · doi:10.7554/elife.83142 · Cited by 45 · 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
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
Metabolic Implications of Circadian–HIF Crosstalk
Peek, C. B. (2020) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2020.02.008 · Cited by 42 · see citing works
The Impact of Shiftwork on Skeletal Muscle Health
Aisbett, B., Condo, D., Zacharewicz, E., & Lamon, S. (2017) · Nutrients · doi:10.3390/nu9030248 · Cited by 38 · 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
Islam, H., Edgett, B. A., Bonafiglia, J. T., Shulman, T., Ma, A., Quadrilatero, J., Simpson, C. A., & Gurd, B. J. (2019) · Experimental Physiology · doi:10.1113/ep087401 · Cited by 38 · see citing works
Daily running enhances molecular and physiological circadian rhythms in skeletal muscle
Casanova-Vallve, N., Duglan, D., Vaughan, M. E., Pariollaud, M., Handzlik, M. K., Fan, W., Yu, R. T., Liddle, C., Downes, M., Delezie, J., et al. (2022) · Molecular Metabolism · doi:10.1016/j.molmet.2022.101504 · Cited by 38 · see citing works
Rossetti, M. L., Esser, K. A., Lee, C., Tomko, R. J., Eroshkin, A. M., & Gordon, B. S. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00177.2019 · Cited by 37 · see citing works
Self-citationCircadian regulation of muscle growth independent of locomotor activity
Kelu, J. J., Pipalia, T. G., & Hughes, S. M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2012450117 · Cited by 37 · see citing works
Ballmann, C. G., Tang, Y., Bush, Z. D., & Rowe, G. C. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00209.2016 · 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
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
The GSK-3β-FBXL21 Axis Contributes to Circadian TCAP Degradation and Skeletal Muscle Function
Wirianto, M., Yang, J., Kim, E., Gao, S., Paudel, K. R., Choi, J. M., Choe, J., Gloston, G. F., Ademoji, P., Parakramaweera, R., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108140 · Cited by 35 · see citing works
Muscle–bone interactions: movement in the field of mechano–humoral coupling of muscle and bone
Cardozo, C. P., & Graham, Z. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13411 · Cited by 31 · see citing works
Riley, L. A., & Esser, K. A. (2017) · Current Osteoporosis Reports · doi:10.1007/s11914-017-0363-2 · Cited by 32 · see citing works
Ze, Y., Wu, Y., Tan, Z., Li, R., Li, R., Gao, W., & Zhao, Q. S. (2025) · Bone Research · doi:10.1038/s41413-025-00403-6 · Cited by 32 · see citing works
Wada, T., Ichihashi, Y., Suzuki, E., Kosuge, Y., Ishige, K., Uchiyama, T., Makishima, M., Nakao, R., Oishi, K., & Shimba, S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092813 · Cited by 32 · 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
Targeted Bmal1 restoration in muscle prolongs lifespan with systemic health effects in aging model
Gutierrez‐Monreal, M. A., Wolff, C. A., Rijos, E. E., Viggars, M. R., Douglas, C. M., Pagala, V., Peng, J., Hunt, L. C., Ding, H., Huo, Z., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.174007 · Cited by 30 · see citing works
Circadian clock genes and respiratory neuroplasticity genes oscillate in the phrenic motor system
Kelly, M. N., Smith, D. N., Sunshine, M. D., Ross, A., Zhang, X., Gumz, M. L., Esser, K. A., & Mitchell, G. S. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00010.2020 · Cited by 30 · 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
Pyle, W. G., & Martino, T. A. (2018) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.05.003 · Cited by 28 · see citing works
Circadian Clock-Controlled Checkpoints in the Pathogenesis of Complex Disease
Li, M., Xin, H., Yuan, Y., Yang, X., Li, H., Tian, D., Zhang, H., Zhang, Z., Han, T.-L., Chen, Q., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.721231 · Cited by 29 · see citing works
Control of circadian muscle glucose metabolism through the BMAL1–HIF axis in obesity
Chaikin, C., Thakkar, A. V., Steffeck, A. W. T., Pfrender, E. M., Hung, K., Zhu, P., Waldeck, N. J., Nozawa, R., Song, W., Futtner, C. R., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2424046122 · Cited by 27 · see citing works
Aoyama, S., Kojima, S., Sasaki, K., Ishikawa, R., Tanaka, M., Shimoda, T., Hattori, Y., Aoki, N., Takahashi, K., Hirooka, R., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.10.057 · Cited by 23 · see citing works
Nakao, R., Shimba, S., & Oishi, K. (2017) · Scientific Reports · doi:10.1038/s41598-017-03119-8 · Cited by 24 · see citing works
Cardiolipin Synthesis in Skeletal Muscle Is Rhythmic and Modifiable by Age and Diet
Nohara, K., Kim, E., Wirianto, M., Mileykovskaya, E., Dowhan, W., Chen, Z., & Yoo, S. H. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5304768 · Cited by 24 · see citing works
Molecular clocks, satellite cells, and skeletal muscle regeneration
Kahn, R. E., Dayanidhi, S., Lacham‐Kaplan, O., & Hawley, J. A. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00073.2023 · Cited by 23 · see citing works
From Chronodisruption to Sarcopenia: The Therapeutic Potential of Melatonin
Fernández‐Martínez, J., Ramírez‐Casas, Y., Yang, Y., Aranda‐Martínez, P., Martínez-Ruiz, L., Escames, G., & Acuña-Castroviejo, D. (2023) · Biomolecules · doi:10.3390/biom13121779 · Cited by 21 · see citing works
Dystrophin deficiency disrupts muscle clock expression and mitochondrial quality control in mdx mice
Hardee, J. P., Caldow, M. K., Chan, A. S. M., Plenderleith, S. K., Trieu, J., Koopman, R., & Lynch, G. S. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00188.2021 · Cited by 20 · see citing works
The skeletal muscle circadian clock regulates titin splicing through RBM20
Riley, L. A., Zhang, X., Douglas, C. M., Mijares, J., Hammers, D. W., Wolff, C. A., Wood, N. B., Olafson, H. R., Du, P., Labeit, S., et al. (2022) · eLife · doi:10.7554/elife.76478 · Cited by 20 · see citing works
BMAL1/PGC1α4-FNDC5/irisin axis impacts distinct outcomes of time-of-day resistance exercise
Guo, M., Shen, F., Guo, X., Zhang, J., Ma, Y., Wu, X., Zuo, H., Yao, J., Hu, Y., Wang, D., et al. (2024) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2024.100968 · Cited by 19 · see citing works
Sweeney, H. L., Masiero, S., & Carraro, U. (2022) · European Journal of Translational Myology · doi:10.4081/ejtm.2022.10440 · Cited by 19 · see citing works
Procopio, S. B., & Esser, K. A. (2024) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2024.11.011 · Cited by 17 · see citing works
Kelu, J. J., & Hughes, S. M. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2422446122 · Cited by 19 · see citing works
Malik, Z. A., Davies, K. A. B., Hall, E. C. R., Barrett, J., Pullinger, S. A., Erskine, R. M., Shepherd, S. O., Iqbal, Z., Edwards, B., & Burniston, J. G. (2020) · Proteomes · doi:10.3390/proteomes8030022 · Cited by 18 · see citing works
Chrono-Nutrition Has Potential in Preventing Age-Related Muscle Loss and Dysfunction
Aoyama, S., Nakahata, Y., & Shinohara, K. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.659883 · Cited by 20 · see citing works
Circadian Rhythm Effects on the Molecular Regulation of Physiological Systems
Crislip, G. R., Johnston, J. G., Douma, L. G., Costello, H. M., Juffre, A., Boyd, K., Li, W. W., Maugans, C. C., Gutierrez‐Monreal, M. A., Esser, K. A., et al. (2021) · Comprehensive physiology · doi:10.1002/cphy.c210011 · Cited by 33 · see citing works
Chrononutrition: Potential, Challenges, and Application in Managing Obesity
Fuad, S. A., Ginting, R. P., & Lee, M.-W. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115116 · Cited by 16 · see citing works
Sutton, E. R., & Pekovic‐Vaughan, V. (2025) · Antioxidants · doi:10.3390/antiox14091132 · Cited by 17 · see citing works
Liang, Q., Lu, Y., Yu, L., Zhu, Q., Xie, W., Wang, Y., Ye, L., Li, Q., Liu, S., Liu, Y., et al. (2021) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-021-01271-w · Cited by 17 · see citing works
Fernández‐Martínez, J., Ramírez‐Casas, Y., Aranda‐Martínez, P., López‐Rodríguez, A., Sayed, R. K. A., Escames, G., & Acuña-Castroviejo, D. (2023) · Journal of Pineal Research · doi:10.1111/jpi.12912 · Cited by 17 · see citing works
Anabolic Heterogeneity Following Resistance Training: A Role for Circadian Rhythm?
CAMERA, D. M. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00569 · Cited by 17 · see citing works
Binge alcohol disrupts skeletal muscle core molecular clock independent of glucocorticoids
Tice, A. L., Laudato, J. A., Rossetti, M. L., Wolff, C. A., Esser, K. A., Lee, C., Lang, C. H., Vied, C., Gordon, B. S., & Steiner, J. L. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00187.2021 · Cited by 16 · see citing works
Dark-light cycle disrupts bone metabolism and suppresses joint deterioration in osteoarthritic rats
Song, X., Zhao, M., Tang, J., Ma, T., Bai, H., Wang, X., Liu, L., Li, T., Xu, X., Sheng, X., et al. (2022) · Arthritis Research & Therapy · doi:10.1186/s13075-022-02832-8 · Cited by 15 · see citing works
Hubbard, E. F., Mashouri, P., Pyle, W. G., & Power, G. A. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00318.2023 · Cited by 15 · see citing works
Montalvão-Sousa, T. M., Ferreira, P. D. A., Colombelli, N. L., de Carvalho, K. M. B., Blazevich, A. J., & Lima, R. M. (2024) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2024.105444 · Cited by 14 · see citing works
Ramírez‐Casas, Y., Fernández‐Martínez, J., Martín‐Estebané, M., Aranda‐Martínez, P., López‐Rodríguez, A., Esquivel‐Ruiz, S., Yang, Y., Escames, G., & Acuña-Castroviejo, D. (2025) · Journal of Pineal Research · doi:10.1111/jpi.70049 · Cited by 14 · see citing works
Chronic Alcohol Consumption Disrupts the Skeletal Muscle Circadian Clock in Female Mice
Tice, A. L., Laudato, J. A., Gordon, B. S., & Steiner, J. L. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221141464 · Cited by 14 · see citing works
Circadian Rhythm Effects on the Molecular Regulation of Physiological Systems
Crislip, G. R., Johnston, J. G., Douma, L. G., Costello, H. M., Juffre, A., Boyd, K., Li, W. W., Maugans, C. C., Gutierrez‐Monreal, M. A., Esser, K. A., et al. (2021) · Comprehensive physiology · doi:10.1002/j.2040-4603.2022.tb00198.x · Cited by 13 · see citing works
Brager, A. J., Heemstra, L. A., Bhambra, R., Ehlen, J. C., Esser, K. A., Paul, K. N., & Novak, C. M. (2016) · Biochimie · doi:10.1016/j.biochi.2016.11.014 · Cited by 13 · see citing works
Extracellular Vesicles and Exosomes in the Control of the Musculoskeletal Health
Penna, F., Garcia‐Castillo, L., & Costelli, P. (2024) · Current Osteoporosis Reports · doi:10.1007/s11914-024-00866-2 · Cited by 12 · see citing works
The role of the circadian timing system in sarcopenia in old age: a scoping review
Palmese, F., Druda, Y., Toro, R. D., Bedogni, G., Domenicali, M., & Silvani, A. (2025) · European Geriatric Medicine · doi:10.1007/s41999-024-01129-0 · Cited by 12 · see citing works
Redox clocks: Time to rethink redox interventions
Nagy, A. D., & Reddy, A. B. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.12.033 · Cited by 12 · see citing works
da Silva, F. M., Cabrera, A. R., Jones, R. G., Schrems, E. R., Muhyudin, R., Washington, T. A., Murach, K. A., & Greene, N. P. (2024) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00647.2024 · Cited by 13 · see citing works
Muscle Bmal1 is Dispensable for the Progress of Neurogenic Muscle Atrophy in Mice
Nakao, R., Shimba, S., & Oishi, K. (2016) · Journal of Circadian Rhythms · doi:10.5334/jcr.141 · Cited by 11 · see citing works
Yusifova, M., Yusifov, A., Polson, S. M., Todd, W. D., Schmitt, E. E., & Bruns, D. R. (2023) · Journal of Biological Rhythms · doi:10.1177/07487304231152398 · Cited by 11 · see citing works
Ye, Z., Huang, K., Dai, X.-Q., Gao, D., Gu, Y., Qian, J., Zhang, F., & Zhai, Q. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e37475 · Cited by 10 · see citing works
Rhythm disturbance in osteoarthritis
Du, Z., You, X., Wu, D., Huang, S., & Zhou, Z. (2022) · Cell Communication and Signaling · doi:10.1186/s12964-022-00891-7 · Cited by 10 · see citing works
Drivers of phenotypic variation in cartilage: Circadian clock genes
Song, X., Bai, H., Meng, X., Xiao, J., & Gao, L. (2021) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16768 · Cited by 10 · see citing works
Circadian Clock in Muscle Disease Etiology and Therapeutic Potential for Duchenne Muscular Dystrophy
Kiperman, T., & Ma, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094767 · Cited by 9 · see citing works
Lack of Bmal1 leads to changes in rhythmicity and impairs motivation towards natural stimuli
Berbegal-Sáez, P., Gallego‐Landin, I., Macía, J., Alegre-Zurano, L., Castro‐Zavala, A., Welz, P.-S., Benitah, S. A., & Valverde, O. (2024) · Open Biology · doi:10.1098/rsob.240051 · Cited by 9 · see citing works
Cancer-induced FOXP1 disrupts and reprograms skeletal-muscle circadian transcription in cachexia
Ducharme, J. B., Neyroud, D., Schonk, M. M., Gutierrez‐Monreal, M. A., Huo, Z., Tucker, H. O., Esser, K. A., Judge, S. M., & Judge, A. R. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115689 · Cited by 9 · see citing works
Apparent Absence of BMAL1-Dependent Skeletal Muscle–Kidney Cross Talk in Mice
Crislip, G. R., Wohlgemuth, S. E., Wolff, C. A., Gutierrez‐Monreal, M. A., Douglas, C. M., Ebrahimi, E., Cheng, K., Masten, S., Barral, D., Bryant, A. J., et al. (2022) · Biomolecules · doi:10.3390/biom12020261 · Cited by 8 · see citing works
Replication and discovery of musculoskeletal QTLs in LG/J and SM/J advanced intercross lines
Cordero, A. I. H., Carbonetto, P. S., Riboni-Verri, G., Gregory, J. S., Vandenbergh, D. J., Gyekis, J. P., Blizard, D. A., & Lionikas, A. (2018) · Physiological Reports · doi:10.14814/phy2.13561 · Cited by 8 · see citing works
Dunlap, K. R., Laskin, G. R., Waddell, D. S., Black, A. J., Steiner, J. L., Vied, C., & Gordon, B. S. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111652 · Cited by 7 · see citing works
Liver as a nexus of daily metabolic cross talk
Litwin, C., & Koronowski, K. B. (2024) · International review of cytology · doi:10.1016/bs.ircmb.2024.06.001 · Cited by 8 · see citing works
Time-of-day effects on ex vivo muscle contractility following short-term satellite cell ablation
Kahn, R. E., Lieber, R. L., Meza, G., Dinnunhan, F., Lacham‐Kaplan, O., Dayanidhi, S., & Hawley, J. A. (2024) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00157.2024 · Cited by 7 · see citing works
The skeletal muscle circadian clock: current insights
Nakao, R., Nikawa, T., & Oishi, K. (2017) · ChronoPhysiology and Therapy · doi:10.2147/cpt.s116569 · Cited by 7 · see citing works
Benefield, D., Abdelmageed, Y., Fowler, J. A., Smith, S., Arias-Parbul, K., Dunning, C., & Rowe, G. C. (2023) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00241.2022 · Cited by 7 · see citing works
Swaminathan, V. R., Rajasundaram, A., & Santhoshkumar, S. (2024) · International Journal of experimental research and review · doi:10.52756/ijerr.2024.v38.010 · Cited by 7 · see citing works
Zhu, P., Chao, C. L., Steffeck, A. W. T., Dang, C., Hamlish, N. X., Pfrender, E. M., Jiang, B., & Peek, C. B. (2024) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.124.321772 · Cited by 6 · see citing works
Muscle-brain crosstalk as a driver of brain health in aging
McNeish, B. L., Miljkovic, I., Liu-Ambrose, T. Y. L., Ambrosio, F., Esser, K. A., Fahnestock, M. L., & Rosano, C. (2025) · GeroScience · doi:10.1007/s11357-025-01833-0 · Cited by 10 · see citing works
- 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
- 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
- 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
- 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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