Cited by 569Circadian rhythm and melatoninDietary Effects on HealthSleep and Work-Related Fatigue

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Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus

Hara, Reiko, Wan, Keiko, Wakamatsu, Hisanori, Aida, Reiko, Moriya, Takahiro, Akiyama, Masashi, Shibata, Shigenobu·2001·Genes to Cells

DOI 10.1046/j.1365-2443.2001.00419.x

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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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Bidirectional interactions between the circadian and reward systems: is restricted food access a unique zeitgeber?
Webb, I. C., Baltazar, R. M., Lehman, M. N., & Coolen, L. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06966.x · Cited by 79
“…the peak of period1 or 2 expression in many of these structures (Wakamatsu et al., 2001; Lamont et al., 2005a; Angeles-Castellanos et al., 2007, 2008; Verwey et al., 2007; Waddington Lamont et al., 2007) without affecting the phase of expression in the SCN (Damiola et al., 2000; Hara et al., 2001).”
Background
Clock genes, intestinal transport and plasma lipid homeostasis
Hussain, M. M., & Pan, X. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.01.001 · Cited by 80
Altered food-anticipatory activity rhythm in Cryptochrome-deficient mice
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“When food is available for only a limited period of daytime (restricted feeding, RF, during 4–7 days), mice, and rats show increased diurnal locomotor activity, 2–4 h before feeding time (Mistlberger, 1994; Hara et al., 2001).”
Background
Beyond the Suprachiasmatic Nucleus
Mrosovsky, N. (2003) · Chronobiology International · doi:10.1081/cbi-120017811 · Cited by 74
“In mice and rats, entrainment both of locomotor activity and of rhythms of gene expression in peripheral organs such as the liver has little or no effect on the rhythm of Per1 expression in the SCN (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
Circadian Rhythms, the Molecular Clock, and Skeletal Muscle
Lefta, M., Wolff, G., & Esser, K. A. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385940-2.00009-7 · Cited by 77
“However, there is growing evidence that peripheral clocks can be synchronized independently of the SCN and that nonphotic timing cues may alternatively entrain peripheral clocks through pathways unknown at this time (Castillo et al., 2004; Hara et al., 2001; Tahara et al. 2010).”
Expression of the circadian clock gene Period 1 in neuroendocrine cells: an investigation using mice with a Per1::GFP transgene
Kriegsfeld, L. J., Korets, R., & Silver, R. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02431.x · Cited by 75
“Email: qr@columbia.edu Received 8 October 2002, revised 29 October 2002, accepted 1 November 2002 present and rhythmic in numerous extra-SCN brain regions (Yamazaki et al., 2000; Abe et al., 2002) as well as in peripheral organs (Damiola et al., 2000; Yamazaki et al., 2000; Hara et al., 2001).”
Background
Ontogeny of Circadian Organization in the Rat
Yamazaki, S., Yoshikawa, T., Biscoe, E. W., Numano, R., Gallaspy, L. M., Soulsby, S. N., Papadimas, E., Pezük, P., Doyle, S. E., Tei, H., et al. (2009) · Journal of Biological Rhythms · doi:10.1177/0748730408328438 · Cited by 72
“While the rhythms of peripheral clocks are usually controlled by the SCN, they can also act independently of the master clock by adjusting their phase in response to exogenous signals such as rhythmic food availability (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
Effects of Fasting and Re-Feeding on the Expression of Dec1, Per1, and Other Clock-Related Genes
Kawamoto, T., Noshiro, M., Furukawa, M., Honda, K. K., Nakashima, A., Ueshima, T., Usui, E., Katsura, Y., Fujimoto, K., Honma, S., et al. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvj165 · Cited by 73
Differential role of the accumbens Shell and Core subterritories in food-entrained rhythms of rats
Mendoza, J., Castellanos, A., & Escobar, C. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.08.016 · Cited by 71
Circadian regulators of intestinal lipid absorption
Hussain, M. M., & Pan, X. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r051573 · Cited by 71
Long-lived αMUPA transgenic mice exhibit pronounced circadian rhythms
Froy, O., Chapnik, N., & Miskin, R. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00140.2006 · Cited by 70
“In turn, calorie intake, energy metabolism, RF, and CR also feed back to the biological clock (4, 13, 29, 40, 48) and help sustain the rhythms.”
Background
Invited Review: A neural clockwork for encoding circadian time
Herzog, E. D., & Schwartz, W. J. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00836.2001 · Cited by 71
Fixing the broken clock in adrenal disorders: focus on glucocorticoids and chronotherapy
Minnetti, M., Hasenmajer, V., Pofi, R., Venneri, M. A., Alexandraki, K., & Isidori, A. M. (2020) · Journal of Endocrinology · doi:10.1530/joe-20-0066 · Cited by 73
Sleep and obesity: A focus on animal models
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The interrelations among feeding, circadian rhythms and ageing
Froy, O., & Miskin, R. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.03.002 · Cited by 74
Melatonin modulates the light-induced sympathoexcitation and vagal suppression with participation of the suprachiasmatic nucleus in mice
Mutoh, T., Shibata, S., Korf, H., & Okamura, H. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.028001 · Cited by 70
Crosstalk between the AHR signaling pathway and circadian rhythm
Shimba, S., & Watabe, Y. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.09.040 · Cited by 74
Effect of intermittent fasting on circadian rhythms in mice depends on feeding time
Froy, O., Chapnik, N., & Miskin, R. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.10.006 · Cited by 70
“contrast with those of restricted feeding (RF) that dictates peripheral rhythms in arrhythmic and mutant mice and animals with lesioned SCN regardless of the lighting conditions (Stephan et al., 1979; Mistlberger, 1994; Hara et al., 2001; Stephan, 2002; Oishi et al., 2002; Horikawa et al., 2005).”
BackgroundResultInfluential
Ablation of AgRP neurons impairs adaption to restricted feeding
Tan, K., Knight, Z. A., & Friedman, J. M. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.07.002 · Cited by 69
Effects of caffeine on circadian phase, amplitude and period evaluated in cells in vitro and peripheral organs in vivo in PER 2:: LUCIFERASE mice
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“As feeding-induced phase shifts of peripheral clocks are independent of SCN oscillation (Hara et al., 2001; Shibata et al., 2010), food or drink containing caffeine may be useful for feeding-induced entrainment of peripheral clocks.”
Background
Time-restricted feeding and the realignment of biological rhythms: translational opportunities and challenges
Sunderram, J., Sofou, S., Kamisoglu, K., Karantza, V., & Androulakis, I. P. (2014) · Journal of Translational Medicine · doi:10.1186/1479-5876-12-79 · Cited by 70
“These works challenge the basic hierarchical paradigm that light entrains the SCN which subsequently entrains the peripheral clocks and emphasized the role of RF as an entraining signal.”
BackgroundInfluential
Eat, Train, Sleep—Retreat? Hormonal Interactions of Intermittent Fasting, Exercise and Circadian Rhythm
Haupt, S., Eckstein, M. L., Wolf, A., Zimmer, R. T., Wachsmuth, N. B., & Moser, O. (2021) · Biomolecules · doi:10.3390/biom11040516 · Cited by 75
“thereby lead to a reset of peripheral clock machinery, leading to shifted phases of peripheral and circadian clocks [105,106].”
Background
Feeding Cues and Injected Nutrients Induce Acute Expression of Multiple Clock Genes in the Mouse Liver
Oike, H., Nagai, K., Fukushima, T., Ishida, N., & Kobori, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023709 · Cited by 72
“Delayed feeding for 13 h is close to the turnaround point because daytime restricted feeding from ZT5 (17 h-delayed) induces a phase advance of the peripheral clock in the mouse [34].”
Effects of chronic forced circadian desynchronization on body weight and metabolism in male mice
Casiraghi, L. P., Alzamendi, A., Giovambattista, A., Chiesa, J. J., & Golombek, D. A. (2016) · Physiological Reports · doi:10.14814/phy2.12743 · Cited by 67
“Even SCN-lesioned mice can recover certain circadian rhythmicity when fed on a periodical schedule (Mendoza 2007).”
BackgroundInfluential
Gene Ontology Mapping as an Unbiased Method for Identifying Molecular Pathways and Processes Affected by Toxicant Exposure: Application to Acute Effects Caused by the Rodent Non-Genotoxic Carcinogen Diethylhexylphthalate
Currie, R. A., Bombail, V., Oliver, J. D., Moore, D. J., Lim, F.-L., Gwilliam, V., Kimber, I., Chipman, K., Moggs, J. G., & Orphanides, G. (2005) · Toxicological Sciences · doi:10.1093/toxsci/kfi207 · Cited by 68
“There is evidence that a number of environmental changes, such as exposure to glucocorticoids and dexamethasone (Balsalobre et al., 2000), as well as food restriction (Hara et al., 2001), may alter the entrainment of the clock in peripheral tissues such as the liver.”
Background
The Role of Mammalian Circadian Proteins in Normal Physiology and Genotoxic Stress Responses
Kondratov, R. V., Gorbacheva, V., & Antoch, M. P. (2007) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(06)78005-x · Cited by 64
Effects of light cues on re-entrainment of the food-dominated peripheral clocks in mammals
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Early nocturnal meal skipping alters the peripheral clock and increases lipogenesis in mice
Yoshida, C., Shikata, N., Seki, S., Koyama, N., & Noguchi, Y. (2012) · Nutrition & Metabolism · doi:10.1186/1743-7075-9-78 · Cited by 68
“Although the SCN clock is mainly regulated by the light/dark cycle, peripheral clock oscillators are affected by daily feeding cycles [23,24].”
BackgroundInfluential
Age-related circadian disorganization caused by sympathetic dysfunction in peripheral clock regulation
Tahara, Y., Takatsu, Y., Shiraishi, T., Kikuchi, Y., Yamazaki, M., Motohashi, H., Muto, A., Sasaki, H., Haraguchi, A., Kuriki, D., et al. (2017) · npj Aging and Mechanisms of Disease · doi:10.1038/npjamd.2016.30 · Cited by 63
“This result is consistent with previous findings indicating that feeding cues are more dominant than light cues for peripheral clock adjustment.(38,39) Thus, we concluded that the maintenance of peripheral clocks in varied lighting conditions was due to the consistency of fasting-feeding cues.”
Result
Nobiletin protects against insulin resistance and disorders of lipid metabolism by reprogramming of circadian clock in hepatocytes
Qi, G., Guo, R., Tian, H., Li, L., Liu, H., Mi, Y., & Liu, X. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.02.009 · Cited by 67
Food as circadian time cue for appetitive behavior
Mistlberger, R. E. (2020) · F1000Research · doi:10.12688/f1000research.20829.1 · Cited by 67
The role of the circadian system in fractal neurophysiological control
Pittman-Polletta, B., Scheer, F. A. J. L., Butler, M. P., Shea, S. A., & Hu, K. (2013) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12032 · Cited by 69
“Recent studies have shown that cells in peripheral organs such as heart and liver have their own circadian clockwork (Balsalobre, Damiola & Schibler, 1998; Damiola et al., 2000; Yamazaki et al., 2000; Hara et al., 2001; Yoo et al., 2004).”
Background
Persistent twenty-four hour changes in liver and bone marrow despite suprachiasmatic nuclei ablation in mice
Filipski, E., King, V. M., Étienne-Grimaldi, M.-C., Li, X., Claustrat, B., Granda, T. G., Milano, G. A., Hastings, M. H., & Lévi, F. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00085.2004 · Cited by 64
“A persistent circadian pattern in the feeding behavior of SCN-lesioned mice kept in LD12:12 may be questioned, as imposed feeding schedules entrained circadian rhythms in the peripheral oscillators of mice with destroyed SCN (18).”
Background
Maternal Feeding Controls Fetal Biological Clock
Ohta, H., Xu, S., Moriya, T., Iigo, M., Watanabe, T., Nakahata, N., Chisaka, H., Hanita, T., Matsuda, T., Ohura, T., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002601 · Cited by 64
“organs [12–14].”
Result
Non‐alcoholic fatty liver disease: the role of nuclear receptors and circadian rhythmicity
Mazzoccoli, G., Vinciguerra, M., Oben, J. A., Tarquini, R., & Cosmo, S. D. (2014) · Liver International · doi:10.1111/liv.12534 · Cited by 66
“In mammals, meal timing drives metabolic activity and clock phase in peripheral tissues (106, 107), and restricted feeding resets the phase of clock gene expression in oscillators located outside the brain (108, 109), but clock gene entrainment by feeding in the various organs shows different grade and speed of reacti…”
Background
Circadian Rhythms and Obesity in Mammals
Froy, O. (2012) · ISRN Obesity · doi:10.5402/2012/437198 · Cited by 66
“RF affects circadian oscillators in peripheral tissues, such as liver, kidney, heart, and pancreas, with no effect on the central pacemaker in the SCN [40, 49, 121, 127, 133, 135, 136].”
BackgroundResult
Effects of meal timing on tumor progression in mice
Wu, M. W., Li, X. M., Xian, L., & Lévi, F. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.02.014 · Cited by 63
Circadian rhythms of clock gene expression in Nile tilapia (Oreochromis niloticus) central and peripheral tissues: influence of different lighting and feeding conditions
Costa, L. S., Serrano-Martínez, I., Sánchez‐Vázquez, F. J., & López‐Olmeda, J. F. (2016) · Journal of Comparative Physiology B · doi:10.1007/s00360-016-0989-x · Cited by 63
“Indeed, the mammalian FEO seems independent of the LEO as the SCN is not required for feeding to entrain rhythms in the livers of SCN-ablated mice (Hara et al. 2001).”
Feeding during the resting phase causes profound changes in physiology and desynchronization between liver and muscle rhythms of rats
Opperhuizen, A., Wang, D., Foppen, E., Jansen, R., Surovtseva, O. V., de Vries, J., Fliers, E., & Kalsbeek, A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13377 · Cited by 64
“Orexin, also known as hypocretin, is an important neurotransmitter in the arousal system (Hara et al., 2001), but also has effects on feeding behavior (Sakurai et al.”
Background
Melatonin induces Nrf2‐HO‐1 reprogramming and corrections in hepatic core clock oscillations in Non‐alcoholic fatty liver disease
Joshi, A., Upadhyay, K. K., Vohra, A., Shirsath, K., & Devkar, R. (2021) · The FASEB Journal · doi:10.1096/fj.202002556rrr · Cited by 63
Central and peripheral circadian clocks and their role in Alzheimer's disease
Chauhan, R., Chen, K.-F., Kent, B. A., & Crowther, D. C. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.030627 · Cited by 58
“Meanwhile, the SCN remains entrained to the light-dark cycle under most conditions (Hara et al., 2001).”
Background
The Association of Energy and Macronutrient Intake at Dinner Versus Breakfast With Disease-Specific and All-Cause Mortality Among People With Diabetes: The U.S. National Health and Nutrition Examination Survey, 2003–2014
Han, T., Gao, J., Wang, L., Li, C., Qi, L., Sun, C., & Li, Y. (2020) · Diabetes Care · doi:10.2337/dc19-2289 · Cited by 60
Regulation of Peripheral Clock to Oscillation of Substance P Contributes to Circadian Inflammatory Pain
Zhang, J., Li, H., Teng, H., Zhang, T., Luo, Y., Zhao, M., Li, Y., & Sun, Z. S. (2012) · Anesthesiology · doi:10.1097/aln.0b013e31825b4fc1 · Cited by 60
“Other studies demonstrated that the peripheral food-entrained clock could overcome the influence of the SCN clock to shift the phase of mouse locomotor activity, further suggesting that some circadian behavior could be controlled by peripheral clock.(3,4) We have now shown that in DRG there is a circadian positive and…”
Background
Systematic analysis of circadian genes using genome-wide cDNA microarrays in the inflammatory bowel disease transcriptome
Palmieri, O., Mazzoccoli, G., Bossa, F., Maglietta, R., Palumbo, O., Ancona, N., Corritore, G., Latiano, T., Martino, G., Rubino, R., et al. (2015) · Chronobiology International · doi:10.3109/07420528.2015.1050726 · Cited by 60
“, 2001), and the phase of clock gene expression is resetted by restricted feeding in peripheral tissues (Damiola et al., 2000; Hara et al., 2001).”
Background
Role of the clock gene Bmal1 and the gastric ghrelin-secreting cell in the circadian regulation of the ghrelin-GOAT system
Laermans, J., Vancleef, L., Tack, J. F., & Depoortere, I. (2015) · Scientific Reports · doi:10.1038/srep16748 · Cited by 60

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
DOI: 10.1046/j.1365-2443.2001.00419.x
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 2685 d)
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 (medical) › 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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Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus

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