Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus
Abstract
BACKGROUND: There are two main stimuli that entrain the circadian rhythm, the light-dark cycle (LD) and restricted feeding (RF). Light-induced entrainment requires induction of the Per1 and Per2 genes in the suprachiasmatic nucleus (SCN), the locus of a main oscillator. In this experiment, we determined whether RF resets the expression of circadian clock genes in the mouse liver with or without participation of the SCN. RESULTS: Mice were allowed access to food for 4 h during the daytime (7 h advance of feeding time) under LD or constant darkness (DD). The peaks of mPer1, mPer2, D-site-binding protein (Dbp) and cholesterol 7alpha-hydroxylase (Cyp7A) mRNA in the liver were advanced 6-12 h after 6 days of RF, whereas those in SCN were unaffected. The advance of mPer expression in the liver by RF was still observed in SCN-lesioned mice. A 7 h advance in the LD cycle advanced the peaks of clock gene expression in both the liver and SCN, whereas, a shift in the LD did not move the phase of the liver clock when the shift was carried out under a fixed RF schedule during the night-time. CONCLUSIONS: These results suggest that restricted feeding strongly entrained the expression of circadian clock genes in the liver without the participation of an SCN clock function.
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In nocturnal rodents, feeding during the daytime hours for a week completely altered the phase of the circadian expression of clock and clock-controlled genes in the peripheral tissues.
“In nocturnal rodents, feeding during the daytime hours for a week completely altered the phase of the circadian expression of clock and clock-controlled genes in the peripheral tissues [261,262].”
From Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance (2022) · cites this paper as [261]
Rhythmic feeding is both necessary and sufficient to drive the circadian expression of liver genes.
“Indeed, it was shown that rhythmic feeding is both necessary and sufficient to drive the circadian expression of liver genes [7,8]”
From Circadian control of glucose metabolism (2014) · cites this paper as [7]
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Sládek, M., Rybová, M., Jindráková, Z., Zemanová, Z., Polidarová, L., Mrnka, L., O'Neill, J. S., Pácha, J., & Sumová, A. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.05.053 · Cited by 156 · see citing works
Clock Genes in Cell Clocks: Roles, Actions, and Mysteries
Okamura, H. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730404269169 · Cited by 157 · see citing works
“This feeding-related entrainment is strong and is observed in SCN-lesioned animals, which indicates that it is independent of the central clock (Hara et al., 2001).”
BackgroundCircadian Rhythms, Aging, and Life Span in Mammals
Froy, O. (2011) · Physiology · doi:10.1152/physiol.00012.2011 · Cited by 156 · see citing works
The role of the circadian clock system in physiology
Pilorz, V., Helfrich‐Förster, C., & Oster, H. (2018) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-2103-y · Cited by 156 · see citing works
“The locus of FEO in the body as well as the underlying mechanism, however, is still poorly understood and subject of ongoing investigations.”
InfluentialCircadian control of root elongation and C partitioning in Arabidopsis thaliana
Yazdanbakhsh, N., Ronan Sulpice, A., Graf, A., Stitt, M., & Fisahn, J. (2011) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2011.02286.x · Cited by 154 · see citing works
Gradients in the circadian expression of Per1 and Per2 genes in the rat suprachiasmatic nucleus
Yan, L., & Okamura, H. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01955.x · Cited by 146 · see citing works
“…has been accumulating that suggests the peripheral tissues also have the SCN-independent circadian oscillating under some special conditions, such as glucocorticoid administration (Balsalobre et al., 1998) or restricted feeding (Damiola et al., 2000; Yamazaki et al., 2000; Hara et al., 2001).”
BackgroundJakubowicz, D., Wainstein, J., Ahrén, B., Bar-Dayan, Y., Landau, Z., Rabinovitz, H. R., & Froy, O. (2015) · Diabetologia · doi:10.1007/s00125-015-3524-9 · Cited by 139 · see citing works
Circadian Dysregulation Disrupts Bile Acid Homeostasis
Ma, K., Xiao, R., Tseng, H.-T., Shan, L., Fu, L., & Moore, D. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006843 · Cited by 144 · see citing works
“As shown in Figure 3A, the expression patterns of Bmal1, Per2, Rev-erba and DBP were all effectively reversed by RF, as expected [2,32].”
InfluentialAKT and TOR Signaling Set the Pace of the Circadian Pacemaker
Zheng, X., & Sehgal, A. (2010) · Current Biology · doi:10.1016/j.cub.2010.05.027 · Cited by 145 · see citing works
Circadian disruption accelerates liver carcinogenesis in mice
Filipski, E., Subramanian, P., Carrière, J., Guettier, C., Barbason, H., & Lévi, F. (2009) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2009.10.002 · Cited by 142 · see citing works
Circadian Rhythms in Diet-Induced Obesity
Engin, A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-48382-5_2 · Cited by 144 · see citing works
“While the SCN directly entrains feeding behavior to the light-dark cycle, daytime feeding shifts the timing of PER expression in the liver (Damiola et al. 2000; Hara et al. 2001).”
BackgroundDisruption of Circadian Coordination and Malignant Growth
Filipski, E., Li, X. M., & Lévi, F. (2006) · Cancer Causes & Control · doi:10.1007/s10552-005-9007-4 · Cited by 141 · see citing works
Mühlbauer, E., Gross, E. C., Labucay, K., Wolgast, S., & Peschke, E. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.01.029 · Cited by 140 · see citing works
“A connection between restricted feeding and organ-internal functions was established by Damiola et al. (2000), Hara et al. (2001) and Stokkan et al. (2001) to be governed by internal clocks in liver, lung and pancreas, as well as by the clocks' interactions with the major oscillator of the nucleus…”
BackgroundDisruption of Circadian Rhythms: A Crucial Factor in the Etiology of Depression
Salgado‐Delgado, R., Osorio, A. T., Saderi, N., & Escobar, C. (2011) · Depression Research and Treatment · doi:10.1155/2011/839743 · Cited by 144 · see citing works
“Although they do not override the light/dark cycle for the adjustment of the SCN, nonphotic stimuli, especially food, contribute as potent synchronizers of cells and organs in the periphery, driving them out of phase from the signals transmitted by the SCN, thus resulting in internal desynchrony [50–52] (Figure 4).”
BackgroundCellular 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
Effect of feeding regimens on circadian rhythms: Implications for agingand longevity
Froy, O., & Miskin, R. (2010) · Aging · doi:10.18632/aging.100116 · Cited by 141 · see citing works
“In turn, some of these functions can feedback to the biological clock in the periphery [143, 153] and the SCN [191, 192] and help sustain the rhythms.”
BackgroundInfluentialJames, F. O., Cermakian, N., & Boivin, D. B. (2007) · Sleep · doi:10.1093/sleep/30.11.1427 · Cited by 135 · see citing works
Husse, J., Leliavski, A., Tsang, A. H., Oster, H., & Eichele, G. (2014) · The FASEB Journal · doi:10.1096/fj.14-256594 · Cited by 133 · see citing works
Verwey, M., Khoja, Z., Stewart, J., & Amir, S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.04.044 · Cited by 132 · see citing works
“, 2005; Mendoza, 2007), suggesting that expression of clock genes in the brain and periphery is not only sensitive to signals from the SCN but also responds to changes in nutritional and/or motivational state independently of the SCN (Hara et al., 2001).”
BackgroundResultInfluentialThe regulation of central and peripheral circadian clocks in humans
Cermakian, N., & Boivin, D. B. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00660.x · Cited by 128 · see citing works
Sakai, R., Hashimoto, Y., Ushigome, E., Miki, A., Okamura, T., Matsugasumi, M., Fukuda, T., Majima, S., Matsumoto, S., Senmaru, T., et al. (2018) · Endocrine Journal · doi:10.1507/endocrj.ej17-0414 · Cited by 132 · see citing works
“Food intake modulates the circadian rhythms, especially in liver and intestine [37, 38] and misalignment of circadian rhythm leads to insulin resistance and diabetes [39, 40].”
BackgroundThe Biological Clock: The Bodyguard of Temporal Homeostasis
Perreau‐Lenz, S., Pévet, P., Buijs, R., & Kalsbeek, A. (2004) · Chronobiology International · doi:10.1081/cbi-120027984 · Cited by 140 · see citing works
“Subsequently, the same clock genes were also found to be expressed rhythmically in other structures, both in the central nervous system (Abe et al., 2002; Yamazaki et al., 2000) and in the periphery (Damiola et al., 2000; Hara et al., 2001; Yamazaki et al., 2000).”
BackgroundEntrainment of the mouse circadian clock by sub-acute physical and psychological stress
Tahara, Y., Shiraishi, T., Kikuchi, Y., Haraguchi, A., Kuriki, D., Sasaki, H., Motohashi, H., Sakai, T., & Shibata, S. (2015) · Scientific Reports · doi:10.1038/srep11417 · Cited by 128 · see citing works
Wible, R. S., Ramanathan, C., Sutter, T. R., Olesen, K. M., Kensler, T. W., Liu, A. C., & Sutter, T. R. (2018) · eLife · doi:10.7554/elife.31656 · Cited by 126 · see citing works
“A predominant entraining signal in peripheral tissues is diurnal metabolic cycles (Hara et al., 2001).”
BackgroundMendoza, J., Castellanos, A., & Escobar, C. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.064 · Cited by 126 · see citing works
Food-entrained circadian rhythms are sustained in arrhythmic Clk/Clk mutant mice
Pitts, S., Perone, E. A., & Silver, R. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00023.2003 · Cited by 126 · see citing works
“the timing of Per expression in the liver in both intact and SCN-lesioned mice (7, 12).”
BackgroundCircadian disruption in experimental cancer processes
Filipski, E., & Lévi, F. (2009) · Integrative Cancer Therapies · doi:10.1177/1534735409352085 · Cited by 125 · see citing works
“To check this hypothesis we used meal timing, which is a strong ZT and was reported to enhance circadian coordination in the liver and in other peripheral organs30,31 even in the absence of functional SCN.32 We inoculated GOS or P03 to mice fed ad libitum and to mice fed only during 4 hours in the light span, from ZT…”
MethodTahara, Y., Otsuka, M., Fuse, Y., Hirao, A., & Shibata, S. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411405958 · Cited by 125 · see citing works
“…cortex can be entrained by restricted feeding stimuli within 2 days, which is the period required before FAA can develop (Damiola et al., 2000; Hara et al., 2001; Wakamatsu et al., 2001; Wu et al., 2004), suggesting a dissociation between the mechanisms of behavioral FAA rhythms and…”
BackgroundInfluentialChronobesity: role of the circadian system in the obesity epidemic
Laermans, J., & Depoortere, I. (2015) · Obesity Reviews · doi:10.1111/obr.12351 · Cited by 126 · see citing works
“So far, brain lesion studies in mice have indicated that loss of several different single brain regions does not completely eliminate FAA (72,73,78,79), implying that rhythmicity is safeguarded by a multitude of FEOs in a number of anatomical locations.”
BackgroundInfluentialMoriya, T., Aida, R., Kudo, T., Akiyama, M., Doi, M., Hayasaka, N., Nakahata, N., Mistlberger, R. E., Okamura, H., & Shibata, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06697.x · Cited by 124 · see citing works
“Notably, food-anticipatory rhythms persist following complete SCN ablation (Stephan et al., 1979; Hara et al., 2001), indicating control by entrainable oscillators located elsewhere (Mistlberger, 1994; Stephan, 2002).”
BackgroundInfluentialMammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Iijima, M., Nikaido, T., Akiyama, M., Moriya, T., & Shibata, S. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02140.x · Cited by 122 · see citing works
“Restricted feeding rapidly entrains the Per gene expression rhythm in the liver (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001) as well as clocks in the cerebral cortex and hippocampus, but not the SCN (Wakamatsu et al., 2001).”
BackgroundSelf-citationGeiger, S. S., Fagundes, C. T., & Siegel, R. M. (2015) · Immunology · doi:10.1111/imm.12525 · Cited by 122 · see citing works
The Cerebellum Harbors a Circadian Oscillator Involved in Food Anticipation
Mendoza, J., Pévet, P., Felder‐Schmittbuhl, M., Bailly, Y. J. R., & Challet, É. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5855-09.2010 · Cited by 122 · see citing works
“Scheduled restricted feeding is a dominant synchronizer for circadian oscillations in peripheral organs, such as the liver (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
BackgroundInteractions between metabolism and circadian clocks: reciprocal disturbances
Delezie, J., & Challet, É. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06246.x · Cited by 118 · see citing works
Cancer Inhibition through Circadian Reprogramming of Tumor Transcriptome with Meal Timing
Li, X., Delaunay, F., Dulong, S., Claustrat, B., Zampera, S., Fujii, Y., Teboul, M., Beau, J., & Lévi, F. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4235 · Cited by 118 · see citing works
Charlot, A., Hutt, F., Sabatier, E., & Zoll, J. (2021) · Nutrients · doi:10.3390/nu13051405 · Cited by 119 · see citing works
Mindikoglu, A. L., Abdulsada, M. M., Jain, A., Choi, J. M., Jalal, P. K., Devaraj, S., Mezzari, M. P., Petrosino, J. F., Opekun, A. R., & Jung, S. Y. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2020.103645 · Cited by 116 · see citing works
“The second mechanism to reset the circadian clock works in response to mealtime during rhythmic, consecutive, time-restricted feeding-fasting cycles.[5, 7, 10] Rhythmic consecutive time-restricted feeding-fasting cycles have shown to release peripheral clocks, including the hepatic clock, from the control of the maste…”
BackgroundInfluentialPeripheral Circadian Clocks in the Vasculature
Reilly, D. F., Westgate, E. J., & FitzGerald, G. A. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.144923 · Cited by 115 · see citing works
Hypothalamic clocks and rhythms in feeding behaviour
Bechtold, D. A., & Loudon, A. S. I. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.12.007 · Cited by 114 · see citing works
Entrainment of the mouse circadian clock: Effects of stress, exercise, and nutrition
Tahara, Y., & Shibata, S. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.12.026 · Cited by 116 · see citing works
“In contrast to the light-dependent central clock, the peripheral clocks can be entrained by food or temperature, even if it is in normal light–dark conditions [14-16].”
BackgroundSun, L., Wang, Y., Song, Y., Cheng, X., Xia, S., Rahman, M. R. T., Shi, Y., & Le, G. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.072 · Cited by 111 · see citing works
The hypothalamic clock and its control of glucose homeostasis
Kalsbeek, A., Yi, C., la Fleur, S. E., & Fliers, E. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2010.02.005 · Cited by 106 · see citing works
“Since it has been shown that a change in feeding pattern has pronounced effects on clock gene expression in the liver (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001), we first investigated whether our 6-meals-a-day feeding schedule affected the normal daily rhythm of clock gene expression in the liver.”
BackgroundOishi, K., Kasamatsu, M., & Ishida, N. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.03.055 · Cited by 107 · see citing works
Role of clock genes in gastrointestinal motility
Hoogerwerf, W. A. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00147.2010 · Cited by 107 · see citing works
- Authors
- Hara, R., Wan, K., Wakamatsu, H., Aida, R., Moriya, T., Akiyama, M., & Shibata, S.
- Affiliations
- Waseda University (JP)
- Corresponding author
- Shibata, Shigenobu
- ORCID
- Shibata, Shigenobu
- Venue
- Genes to Cells
- Publisher
- Wiley
- Published
- 2001-03
- Volume
- 6
- Issue
- 3
- Pages
- 269-278
- ISSN
- 1356-9597 (ISSN-L)
- 1365-2443
- OpenAlex
- W1965036088
- Cited by
- 569
- References
- 28
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 17 · 2023: 20 · 2022: 27 · 2021: 24 · 2020: 24 · 2019: 18 · 2018: 23 · 2017: 36 · 2016: 20 · 2015: 29 · 2014: 26 · 2013: 21 · 2012: 29
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Genes to Cells (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerul Cercetării, Inovării şi Digitalizării
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- feed restriction, circadian entrainment, liver clock, suprachiasmatic nucleus, clock genes, Per1, Per2, DBP, SCN lesions, light-dark cycle, constant darkness
- MeSH terms
- Animals, Biological Clocks, Feeding Methods, Gene Expression Regulation, Liver, Male, Nuclear Proteins, Suprachiasmatic Nucleus, Transcription Factors, Cell Cycle Proteins, Mice, Period Circadian Proteins
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