The skeletal muscle circadian clock: current insights

References

• Bowen TS, Schuler G, Adams V. Skeletal muscle wasting in cachexia and sarcopenia: molecular pathophysiology and impact of exercise training. J Cachexia Sarcopenia Muscle. 2015;6(3):197–207.
   PubMed Web of Science ®Google Scholar
• Yu JH, Yun CH, Ahn JH, et al. Evening chronotype is associated with metabolic disorders and body composition in middle-aged adults. J Clin Endocrinol Metab. 2015;100(4):1494–1502.
   PubMed Web of Science ®Google Scholar
• Di Lorenzo L, De Pergola G, Zocchetti C, et al. Effect of shift work on body mass index: results of a study performed in 319 glucose-tolerant men working in a Southern Italian industry. Int J Obes Relat Metab Disord. 2003;27(11):1353–1358.
   Web of Science ®Google Scholar
• Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A. 1972;69(6):1583–1586.
   PubMed Web of Science ®Google Scholar
• Drucker-Colin R, Aguilar-Roblero R, Garcia-Hernandez F, Fernandez-Cancino F, Bermudez Rattoni F. Fetal suprachiasmatic nucleus transplants: diurnal rhythm recovery of lesioned rats. Brain Res. 1984;311(2):353–357.
   PubMed Web of Science ®Google Scholar
• Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990;247(4945):975–978.
   PubMed Web of Science ®Google Scholar
• Colwell CS, Foster RG. Photic regulation of Fos-like immunoreactivity in the suprachiasmatic nucleus of the mouse. J Comp Neurol. 1992;324(2):135–142.
   Web of Science ®Google Scholar
• Meijer JH, Schwartz WJ. In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J Biol Rhythms. 2003;18(3):235–249.
   Web of Science ®Google Scholar
• Buhr ED, Takahashi JS. Molecular components of the mammalian circadian clock. Handb Exp Pharmacol. 2013(217):3–27.
   Google Scholar
• Dardente H, Cermakian N. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int. 2007;24(2):195–213.
   PubMed Web of Science ®Google Scholar
• Eide EJ, Vielhaber EL, Hinz WA, Virshup DM. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon. J Biol Chem. 2002;277(19):17248–17254.
   PubMed Web of Science ®Google Scholar
• Lee C, Etchegaray JP, Cagampang FR, Loudon AS, Reppert SM. Posttranslational mechanisms regulate the mammalian circadian clock. Cell. 2001;107(7):855–867.
   PubMed Web of Science ®Google Scholar
• Lowrey PL, Shimomura K, Antoch MP, et al. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science. 2000;288(5465):483–492.
   Web of Science ®Google Scholar
• Eide EJ, Woolf MF, Kang H, et al. Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol Cell Biol. 2005;25(7):2795–2807.
   PubMed Web of Science ®Google Scholar
• Busino L, Bassermann F, Maiolica A, et al. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science. 2007;316(5826):900–904.
   PubMed Web of Science ®Google Scholar
• Preitner N, Damiola F, Lopez-Molina L, et al. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 2002;110(2):251–260.
   PubMed Web of Science ®Google Scholar
• Sato TK, Panda S, Miraglia LJ, et al. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron. 2004;43(4):527–537.
   PubMed Web of Science ®Google Scholar
• Guillaumond F, Dardente H, Giguere V, Cermakian N. Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms. 2005;20(5):391–403.
   PubMed Web of Science ®Google Scholar
• Crumbley C, Burris TP. Direct regulation of CLOCK expression by REV-ERB. PLoS One. 2011;6(3):e17290.
   PubMed Web of Science ®Google Scholar
• Yamazaki S, Numano R, Abe M, et al. Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000;288(5466):682–685.
   PubMed Web of Science ®Google Scholar
• Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U. Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell. 2004;119(5):693–705.
   PubMed Web of Science ®Google Scholar
• Yoo SH, Yamazaki S, Lowrey PL, et al. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A. 2004; 101(15):5339–5346.
   PubMed Web of Science ®Google Scholar
• Panda S, Antoch MP, Miller BH, et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002;109(3):307–320.
   PubMed Web of Science ®Google Scholar
• Ueda HR, Chen W, Adachi A, et al. A transcription factor response element for gene expression during circadian night. Nature. 2002;418(6897):534–539.
   PubMed Web of Science ®Google Scholar
• Storch KF, Lipan O, Leykin I, et al. Extensive and divergent circadian gene expression in liver and heart. Nature. 2002;417(6884):78–83.
   PubMed Web of Science ®Google Scholar
• Miller BH, McDearmon EL, Panda S, et al. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci U S A. 2007;104(9):3342–3347.
   PubMed Web of Science ®Google Scholar
• Zylka MJ, Shearman LP, Weaver DR, Reppert SM. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron. 1998;20(6):1103–1110.
   PubMed Web of Science ®Google Scholar
• McCarthy JJ, Andrews JL, McDearmon EL, et al. Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol Genomics. 2007;31(1):86–95.
   PubMed Web of Science ®Google Scholar
• McWatters H, Dunlap JC, Millar AJ. Circadian biology: clocks for the real world. Curr Biol. 1999;9(17):R633–R635.
   Web of Science ®Google Scholar
• Roenneberg T, Merrow M. Circadian clocks – from genes to complex behaviour. Reprod Nutr Dev. 1999;39(3):277–294.
   Google Scholar
• Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000;14(23):2950–2961.
   PubMed Web of Science ®Google Scholar
• Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science. 2001;291(5503):490–493.
   PubMed Web of Science ®Google Scholar
• Guo H, Brewer JM, Champhekar A, Harris RB, Bittman EL. Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci U S A. 2005;102(8):3111–3116.
   PubMed Web of Science ®Google Scholar
• Hara R, Wan K, Wakamatsu H, et al. Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells. 2001;6(3):269–278.
   PubMed Web of Science ®Google Scholar
• Yasumoto Y, Hashimoto C, Nakao R, et al. Short-term feeding at the wrong time is sufficient to desynchronize peripheral clocks and induce obesity with hyperphagia, physical inactivity and metabolic disorders in mice. Metabolism. 2016;65(5):714–727.
   Web of Science ®Google Scholar
• Oishi K, Yasumoto Y, Higo-Yamamoto S, Yamamoto S, Ohkura N. Feeding cycle-dependent circulating insulin fluctuation is not a dominant Zeitgeber for mouse peripheral clocks except in the liver: differences between endogenous and exogenous insulin effects. Biochem Biophys Res Commun. 2017;483(1):165–170.
   Web of Science ®Google Scholar
• Reebs SG, Mrosovsky N. Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J Biol Rhythms. 1989;4(1):39–48.
   PubMed Web of Science ®Google Scholar
• Marchant EG, Mistlberger RE. Entrainment and phase shifting of circadian rhythms in mice by forced treadmill running. Physiol Behav. 1996;60(2):657–663.
   Web of Science ®Google Scholar
• Zambon AC, McDearmon EL, Salomonis N, et al. Time- and exercise-dependent gene regulation in human skeletal muscle. Genome Biol. 2003;4(10):R61.
   PubMed Web of Science ®Google Scholar
• Wolff G, Esser KA. Scheduled exercise phase shifts the circadian clock in skeletal muscle. Med Sci Sports Exerc. 2012;44(9):1663–1670.
   Web of Science ®Google Scholar
• Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159(4):738–749.
   PubMed Web of Science ®Google Scholar
• Balsalobre A, Brown SA, Marcacci L, et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000; 289(5488):2344–2347.
   PubMed Web of Science ®Google Scholar
• Yasumoto Y, Nakao R, Oishi K. Free access to a running-wheel advances the phase of behavioral and physiological circadian rhythms and peripheral molecular clocks in mice. PLoS One. 2015;10(1):e0116476.
   Web of Science ®Google Scholar
• Droste SK, Gesing A, Ulbricht S, Muller MB, Linthorst AC, Reul JM. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology. 2003;144(7):3012–3023.
   PubMed Web of Science ®Google Scholar
• Sasaki H, Hattori Y, Ikeda Y, et al. Phase shifts in circadian peripheral clocks caused by exercise are dependent on the feeding schedule in PER2::LUC mice. Chronobiol Int. 2016;33(7):849–862.
   PubMed Web of Science ®Google Scholar
• Nakao R, Yamamoto S, Horikawa K, et al. Atypical expression of circadian clock genes in denervated mouse skeletal muscle. Chronobiol Int. 2015;32(4):486–496.
   PubMed Web of Science ®Google Scholar
• Dyar KA, Ciciliot S, Tagliazucchi GM, et al. The calcineurin-NFAT pathway controls activity-dependent circadian gene expression in slow skeletal muscle. Mol Metab. 2015;4(11):823–833.
   PubMed Web of Science ®Google Scholar
• Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 2006;20(14):1868–1873.
   PubMed Web of Science ®Google Scholar
• Andrews JL, Zhang X, McCarthy JJ, et al. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci U S A. 2010;107(44):19090–19095.
   PubMed Web of Science ®Google Scholar
• Dyar KA, Ciciliot S, Wright LE, et al. Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol Metab. 2014;3(1):29–41.
   PubMed Web of Science ®Google Scholar
• Nakao R, Shimba S, Oishi K. Muscle Bmal1 is dispensable for the progress of neurogenic muscle atrophy in mice. J Circadian Rhythms. 2016;14(1):6.
   Google Scholar
• Schroder EA, Harfmann BD, Zhang X, et al. Intrinsic muscle clock is necessary for musculoskeletal health. J Physiol. 2015;593(24):5387–5404.
   PubMed Web of Science ®Google Scholar
• Nyberg M, Hellsten Y. Reduced blood flow to contracting skeletal muscle in ageing humans: is it all an effect of sand through the hourglass? J Physiol. 2016;594(8):2297–2305.
   Web of Science ®Google Scholar
• Gomes MJ, Martinez PF, Pagan LU, et al. Skeletal muscle aging: influence of oxidative stress and physical exercise. Oncotarget. 2017;8(12):20428–20440.
   PubMedGoogle Scholar
• Jacobi D, Liu S, Burkewitz K, et al. Hepatic Bmal1 regulates rhythmic mitochondrial dynamics and promotes metabolic fitness. Cell Metab. 2015;22(4):709–720.
   PubMed Web of Science ®Google Scholar
• Yang G, Chen L, Grant GR, et al. Timing of expression of the core clock gene Bmal1 influences its effects on aging and survival. Sci Transl Med. 2016;8(324):324ra316.
   Web of Science ®Google Scholar
• Dolatshad H, Cary AJ, Davis FC. Differential expression of the circadian clock in maternal and embryonic tissues of mice. PLoS One. 2010;5(3):e9855.
   Web of Science ®Google Scholar
• Lipton JO, Yuan ED, Boyle LM, et al. The circadian protein BMAL1 regulates translation in response to S6K1-mediated phosphorylation. Cell. 2015;161(5):1138–1151.
   PubMed Web of Science ®Google Scholar
• Hodge BA, Wen Y, Riley LA, et al. The endogenous molecular clock orchestrates the temporal separation of substrate metabolism in skeletal muscle. Skelet Muscle. 2015;5:17.
   PubMed Web of Science ®Google Scholar
• Doherty TJ. Invited review: aging and sarcopenia. J Appl Physiol. 2003;95(4):1717–1727.
   PubMedGoogle Scholar
• Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21(4):543–559.
   PubMed Web of Science ®Google Scholar
• Wakabayashi H, Sakuma K. Comprehensive approach to sarcopenia treatment. Curr Clin Pharmacol. 2014;9(2):171–180.
   Google Scholar
• Ballesta A, Innominato PF, Dallmann R, Rand DA, Levi FA. Systems chronotherapeutics. Pharmacol Rev. 2017;69(2):161–199.
   PubMed Web of Science ®Google Scholar
• Levi F, Okyar A, Dulong S, Innominato PF, Clairambault J. Circadian timing in cancer treatments. Annu Rev Pharmacol Toxicol. 2010;50:377–421.
   PubMed Web of Science ®Google Scholar
• Levi FA, Boige V, Hebbar M, et al. Conversion to resection of liver metastases from colorectal cancer with hepatic artery infusion of combined chemotherapy and systemic cetuximab in multicenter trial OPTILIV. Ann Oncol. 2016;27(2):267–274.
   PubMed Web of Science ®Google Scholar
• Ranjan OP, Nayak UY, Reddy MS, Dengale SJ, Musmade PB, Udupa N. Osmotically controlled pulsatile release capsule of montelukast sodium for chronotherapy: statistical optimization, in vitro and in vivo evaluation. Drug Deliv. 2014;21(7):509–518.
   PubMed Web of Science ®Google Scholar
• Smolensky MH, Hermida RC, Ayala DE, Portaluppi F. Bedtime hypertension chronotherapy: concepts and patient outcomes. Curr Pharm Des. 2015;21(6):773–790.
   Web of Science ®Google Scholar
• Hermida RC, Ayala DE, Mojon A, Fernandez JR. Influence of circadian time of hypertension treatment on cardiovascular risk: results of the MAPEC study. Chronobiol Int. 2010;27(8):1629–1651.
   PubMed Web of Science ®Google Scholar
• Hermida RC, Ayala DE, Fernandez JR, Portaluppi F, Fabbian F, Smolensky MH. Circadian rhythms in blood pressure regulation and optimization of hypertension treatment with ACE inhibitor and ARB medications. Am J Hypertens. 2011;24(4):383–391.
   Web of Science ®Google Scholar
• Hermida RC, Ayala DE, Mojon A, Fernandez JR. Bedtime dosing of antihypertensive medications reduces cardiovascular risk in CKD. J Am Soc Nephrol. 2011;22(12):2313–2321.
   PubMed Web of Science ®Google Scholar
• Roush GC, Fapohunda J, Kostis JB. Evening dosing of antihypertensive therapy to reduce cardiovascular events: a third type of evidence based on a systematic review and meta-analysis of randomized trials. J Clin Hypertens. 2014;16(8):561–568.
   PubMed Web of Science ®Google Scholar
• Nakao R, Yamamoto S, Yasumoto Y, Oishi K. Dosing schedule-dependent attenuation of dexamethasone-induced muscle atrophy in mice. Chronobiol Int. 2014;31(4):506–514.
   PubMed Web of Science ®Google Scholar
• Oike H, Oishi K, Kobori M. Nutrients, clock genes, and chrononutrition. Current Nutr Rep. 2014;3:204–212.
   PubMedGoogle Scholar
• Tahara Y, Shibata S. Chronobiology and nutrition. Neuroscience. 2013;253:78–88.
   PubMed Web of Science ®Google Scholar
• Johnston JD, Ordovas JM, Scheer FA, Turek FW. Circadian rhythms, metabolism, and chrononutrition in rodents and humans. Adv Nutr. 2016;7(2):399–406.
   PubMed Web of Science ®Google Scholar
• Oike H. Modulation of circadian clocks by nutrients and food factors. Biosci Biotechnol Biochem. 2017;81(5):863–870.
   PubMed Web of Science ®Google Scholar
• Mamerow MM, Mettler JA, English KL, et al. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. J Nutr. 2014;144(6):876–880.
   PubMed Web of Science ®Google Scholar
• Murphy CH, Churchward-Venne TA, Mitchell CJ, et al. Hypoenergetic diet-induced reductions in myofibrillar protein synthesis are restored with resistance training and balanced daily protein ingestion in older men. Am J Physiol Endocrinol Metab. 2015;308(9):E734–E743.
   Web of Science ®Google Scholar
• Pan X, Terada T, Irie M, Saito H, Inui K. Diurnal rhythm of H+-peptide cotransporter in rat small intestine. Am J Physiol Gastrointest Liver Physiol. 2002;283(1):G57–G64.
   PubMed Web of Science ®Google Scholar
• Pan X, Terada T, Okuda M, Inui K. Altered diurnal rhythm of intestinal peptide transporter by fasting and its effects on the pharmacokinetics of ceftibuten. J Pharmacol Exp Ther. 2003;307(2):626–632.
   PubMed Web of Science ®Google Scholar
• Zhang X, Dube TJ, Esser KA. Working around the clock: circadian rhythms and skeletal muscle. J Appl Physiol. 2009;107(5):1647–1654.
   PubMed Web of Science ®Google Scholar
• Souissi N, Gauthier A, Sesboue B, Larue J, Davenne D. Effects of regular training at the same time of day on diurnal fluctuations in muscular performance. J Sports Sci. 2002;20(11):929–937.
   PubMed Web of Science ®Google Scholar
• Sedliak M, Finni T, Peltonen J, Hakkinen K. Effect of time-of-day-specific strength training on maximum strength and EMG activity of the leg extensors in men. J Sports Sci. 2008;26(10):1005–1014.
   PubMed Web of Science ®Google Scholar
• Sedliak M, Finni T, Cheng S, Lind M, Hakkinen K. Effect of time-of-day-specific strength training on muscular hypertrophy in men. J Strength Cond Res. 2009;23(9):2451–2457.
   PubMed Web of Science ®Google Scholar
• Pastore S, Hood DA. Endurance training ameliorates the metabolic and performance characteristics of circadian Clock mutant mice. J Appl Physiol. 2013;114(8):1076–1084.
   Web of Science ®Google Scholar
• Aoyama S, Shibata S. The role of circadian rhythms in muscular and osseous physiology and their regulation by nutrition and exercise. Front Neurosci. 2017;11:63.
   PubMed Web of Science ®Google Scholar