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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Background
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Background
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Effect of upregulated renin–angiotensin system on per2 and bmal1 gene expression in brain structures involved in blood pressure control in TGR(mREN-2)27 rats
Monošíková, J., Herichová, I., Mravec, B., Kiss, A., & Zeman, M. (2007) · Brain Research · doi:10.1016/j.brainres.2007.08.061 · Cited by 20
Circadian Clocks for All Meal-Times: Anticipation of 2 Daily Meals in Rats
Mistlberger, R. E., Kent, B. A., Chan, S., Patton, D. F., Weinberg, A., & Parfyonov, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031772 · Cited by 20
“First, it has been shown repeatedly that in LDentrained rats, the SCN is not phase shifted by daytime feeding schedules [33–37].”
Background
Circadian Rhythm of Lipid Metabolism in Health and Disease
Zhang, Z., Xin, H., & Li, M. (2020) · Small Methods · doi:10.1002/smtd.201900601 · Cited by 21
Entrainment of mouse peripheral circadian clocks to <24 h feeding/fasting cycles under 24 h light/dark conditions
Hamaguchi, Y., Tahara, Y., Kuroda, H., Haraguchi, A., & Shibata, S. (2015) · Scientific Reports · doi:10.1038/srep14207 · Cited by 20
l-Ornithine affects peripheral clock gene expression in mice
Fukuda, T., Haraguchi, A., Kuwahara, M., Nakamura, K., Hamaguchi, Y., Ikeda, Y., Ishida, Y., Wang, G., Shirakawa, C., Tanihata, Y., et al. (2016) · Scientific Reports · doi:10.1038/srep34665 · Cited by 21
Two-peaked Synchronization in Day/Night Expression Rhythms of the Fibrinogen Gene Cluster in the Mouse Liver
Sakao, E., Ishihara, A., Horikawa, K., Akiyama, M., Arai, M., Kato, M., Seki, N., Fukunaga, K., Shimizu-Yabe, A., Iwase, K., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304809200 · Cited by 24
Altered expression profiles of clock genes hPer1 and hPer2 in peripheral blood mononuclear cells of cancer patients undergoing surgery
Azama, T., Yano, M., Oishi, K., Kadota, K., Hyun, K., Tokura, H., Nishimura, S., Matsunaga, T., Iwanaga, H., Miki, H., et al. (2006) · Life Sciences · doi:10.1016/j.lfs.2006.11.048 · Cited by 19
Scheduled meal accelerates entrainment to a 6‐h phase advance by shifting central and peripheral oscillations in rats
Ubaldo-Reyes, L. M., Buijs, R. M., Escobar, C., & Ángeles‐Castellanos, M. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13633 · Cited by 20
“E-mail: mangeles_castellanos@unam.mx © 2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd tissues (Hara et al., 2001; Mukherji et al., 2015), as well as neuronal activity rhythms in the hypothalamus ( Angeles-Castellanos et al., 2004; Gooley et al., 2006), corticolimbic…”
Background
Misaligned Feeding May Aggravate Pain by Disruption of Sleep–Awake Rhythm
Xu, F., Zhao, X., Liu, H., Shao, X., Chu, S., Gong, X., Ma, Z., & Gu, X. (2017) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000002727 · Cited by 19
Deregulated expression of the per2 gene in human colorectal carcinoma
Zeman, M., Vician, M., Monošíková, J., Reis, R. D. F., & Herichová, I. (2008) · Molecular Medicine Reports · doi:10.3892/mmr.1.4.599 · Cited by 19
RATS MADE CIRRHOTIC BY CHRONIC CCl4TREATMENT STILL EXHIBIT ANTICIPATORY ACTIVITY TO A RESTRICTED FEEDING SCHEDULE
Escobar, C., Mendoza, J., Salazar‐Juárez, A., Ávila, J. M. R., Hernández-Muñoz, R. E., Díaz‐Muñoz, M., & Aguilar‐Roblero, R. A. (2002) · Chronobiology International · doi:10.1081/cbi-120015964 · Cited by 19
“Entrainment to RFS of clock genes in the liver has also been observed in SCN-lesioned mice, although their food-entrained phase is not modified by shifts in the LD cycle.([20]) These data support the probability that the liver plays an important role as a biological oscillator for the FEO.”
Background
Time Restricted Eating: A Valuable Alternative to Calorie Restriction for Addressing Obesity?
Parrotta, M. E., Colangeli, L., Scipione, V., Vitale, C., Sbraccia, P., & Guglielmi, V. (2025) · Current Obesity Reports · doi:10.1007/s13679-025-00609-z · Cited by 19
Finding balance: understanding the energetics of time‐restricted feeding in mice
Gallop, M. R., Tobin, S. Y., & Chaix, A. (2022) · Obesity · doi:10.1002/oby.23607 · Cited by 19
Differential Patterns in the Periodicity and Dynamics of Clock Gene Expression in Mouse Liver and Stomach
Mazzoccoli, G., Francavilla, M., Pazienza, V., Benegiamo, G., Piepoli, A., Vinciguerra, M., Giuliani, F., Yamamoto, T., & Takumi, T. (2012) · Chronobiology International · doi:10.3109/07420528.2012.728662 · Cited by 19
“…through the release of circulating systemic factors (melatonin, glucocorticoids), but periodic food availability, provided by scheduled restricted feeding, is the dominant synchronizer for peripheral clocks, such as liver and gut (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
The human circadian clock from health to economics
Koritala, B. S. C., & Çakmaklı, S. (2018) · PsyCh Journal · doi:10.1002/pchj.252 · Cited by 16
Stress affects expression of the clock gene Bmal1 in the suprachiasmatic nucleus of neonatal rats via glucocorticoid‐dependent mechanism
Olejníková, L., Polidarová, L., & Sumová, A. (2017) · Acta Physiologica · doi:10.1111/apha.13020 · Cited by 18
“The reactivity of the circadian clock in the SCN to stressful stimuli has been controversial, but most studies have confirmed the resilience of the SCN to stress.(12,13) This resilience has been explained by the numerous observations that the adult SCN is nearly devoid of GRs.”
Background
Resetting the Aging Clock: Implications for Managing Age-Related Diseases
Nobrega, A. K. D., Luz, K. V., & Lyons, L. C. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-42667-5_9 · Cited by 20
Feeding Schedule Controls Circadian Timing of Daily Torpor in SCN-Ablated Siberian Hamsters
Paul, M. J., Kauffman, A. S., & Zucker, I. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730404264337 · Cited by 18
Resetting Process of Peripheral Circadian Gene Expression after the Combined Reversal of Feeding Schedule and Light/Dark Cycle Via a 24-h Light Period Transition in Rats
Wu, T., Ni, Y., Zhuge, F., & Fu, Z. (2010) · Physiological Research · doi:10.33549/physiolres.931818 · Cited by 18
Chronic circadian desynchronization of feeding-fasting rhythm generates alterations in daily glycemia, LDL cholesterolemia and microbiota composition in mice
Trebucq, L. L., Lamberti, M. L., Rota, R. P., Aiello, I., Borio, C. S., Bilen, M. F., Golombek, D. A., Plano, S. A., & Chiesa, J. J. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1154647 · Cited by 19
“Feedback signals from the feeding-fasting rhythm act as strong zeitgebers (synchronizers) for oscillators in metabolic tissues controlling energy homeostasis, indeed bypassing the SCN under time-restricted feeding protocols (4), or without its participation (5).”
Background
Differential responses of peripheral circadian clocks to a short-term feeding stimulus
Wu, T., Fu, O., Yao, L., Sun, L., ZhuGe, F., & Fu, Z. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1844-0 · Cited by 16
Rhythm is essential: Unraveling the relation between the circadian clock and cancer
Ogunlusi, O., Ghosh, A., Sarkar, M., Carter, K., Davuluri, H., Chakraborty, M., Eckel‐Mahan, K. L., Keene, A. C., Menet, J. S., Bell‐Pedersen, D., et al. (2025) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2025.104632 · Cited by 17
Mathematical analysis of circadian disruption and metabolic re-entrainment of hepatic gluconeogenesis: the intertwining entraining roles of light and feeding
Bae, S.-A., & Androulakis, I. P. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00271.2017 · Cited by 16
“dPGC-1 dt kg3b · PGC-1 mRNA kg3d · PGC-1 kg3t · PGC-1 kg4t · PGC-1 (N) (11)”
Background
Mediators of Host–Microbe Circadian Rhythms in Immunity and Metabolism
Frazier, K., Frith, M., Harris, D., & Leone, V. (2020) · Biology · doi:10.3390/biology9120417 · Cited by 16
“Conversely, TRF to the rest phase in mice disrupts natural sleep and behavioral patterns, resulting in major disruptions of host gene expression, particularly in liver, independent of the central clock [59].”
Background
All-trans retinoic acid modifies the expression of clock and disease marker genes
Sherman, H., Gutman, R., Chapnik, N., Meylan, J., le Coutre, J., & Froy, O. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2010.11.017 · Cited by 18
Mystery of rhythmic signal emergence within the suprachiasmatic nuclei
Sumová, A., & Čečmanová, V. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14141 · Cited by 17
“Intriguingly, although the adult SCN is mostly insensitive to changes in the feeding regime (Damiola et al., 2000; Hara et al., 2001), the fetal SCN clock can sense the change in maternal feeding behavior and can adjust its phase accordingly.”
Background
Multiomics analyses reveal dynamic bioenergetic pathways and functional remodeling of the heart during intermittent fasting
Arumugam, T. V., Shaik, A. A., Liehn, E. A., Selvaraji, S., Poh, L., Rajeev, V., Cho, Y., Cho, Y. E., Kim, J.-H., Kim, J., et al. (2023) · eLife · doi:10.7554/elife.89214.2 · Cited by 15
Mistimed wheel running interferes with re‐entrainment of circadian Per1 rhythms in the mouse skeletal muscle and lung
Yamanaka, Y., Honma, S., & Honma, K. (2016) · Genes to Cells · doi:10.1111/gtc.12336 · Cited by 15
“A similar acceleration has been observed by timed RF (Hara et al. 2001; Angeles-Castellanos et al. 2011), in which animals ran a running wheel vigorously before daily meal and developed the so-called prefeeding or anticipatory activity (Mistlberger 1994).”
BackgroundMethodInfluential
Proteomic changes in the hypothalamus and retroperitoneal fat from male F344 rats subjected to repeated light–dark shifts
Mishra, A., Cheng, C., Lee, W., & Tsai, L. (2009) · PROTEOMICS · doi:10.1002/pmic.200800813 · Cited by 15
Daily rhythms are retained both in spontaneously developed sarcomas and in xenografts grown in immunocompromised SCID mice
Comas, M., Kuropatwinski, K. K., Wrobel, M. M., Toshkov, I. A., & Antoch, M. P. (2014) · Chronobiology International · doi:10.3109/07420528.2014.925469 · Cited by 15
“…have shown that food availability is an SCN-independent synchronizing cue for the liver and, as a consequence, restricting food administration to the rest period of the circadian cycle alters the phase relationship between liver and SCN (Damiola, 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
Conditional postnatal deletion of the neonatal murine hepatic circadian gene, Npas2, alters the gut microbiome following restricted feeding
O’Neil, D. S., Stewart, C. J., Chu, D. M., Goodspeed, D. M., Gonzalez‐Rodriguez, P. J., Shope, C. D., & Aagaard, K. M. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.03.024 · Cited by 15
“Therefore, when Npas2 is not functioning the 384 entrainment of mouse feeding behavior occurs through the SCN, whose circadian rhythm is not entrained through external 385 feeding cues, but instead through light/dark cues (58).”
Background
Non-photic circadian entrainment in mammals: A brief review and proposal for study during development
Caldelas, I., Chimal‐Monroy, J., Martı́nez–Gómez, M., & Hudson, R. (2005) · Biological Rhythm Research · doi:10.1080/09291010400028500 · Cited by 14
“At the molecular level timed provision of the normal daily food ration to mice maintained in constant darkness has no effect on the rhythmic expression of clock genes in the SCN (Damiola et al., 2000; Hara et al., 2001; Wakamatsu et al., 2001).”
Background
Different levels of circadian (de)synchrony – where does it hurt?
Galinde, A. A., Al‐Μughales, F., Oster, H., & Heyde, I. (2022) · F1000Research · doi:10.12688/f1000research.127234.2 · Cited by 13
Circadian PER1 controls daily fat absorption with the regulation of PER1-PKA on phosphorylation of bile acid synthetase
Ge, W., Sun, Q., Yang, Y., Ding, Z., Liu, J., & Zhang, J. (2023) · Journal of Lipid Research · doi:10.1016/j.jlr.2023.100390 · Cited by 13
“Followed restricted feeding schedules, several physiological functions and variables occur before eating, preparing to anticipate food intake and being synchronized (8).”
Background
Peripheral clock gene expression in CS mice with bimodal locomotor rhythms
Watanabe, T., Kojima, M., Tomida, S., Nakamura, T. J., Yamamura, T., Nakao, N., Yasuo, S., Yoshimura, T., & Ebihara, S. (2006) · Neuroscience Research · doi:10.1016/j.neures.2005.12.009 · Cited by 13
“Among several time cues to entrain peripheral rhythms, feeding has been known as a dominant synchronizer, but this does not affect the phase of the SCN (Damiola et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
Enhanced effect of daytime restricted feeding on the circadian rhythm of streptozotocin-induced type 2 diabetic rats
Wu, T., Zhuge, F., Sun, L. Z., Ni, Y., Fu, O., Gao, G., Chen, J., Kato, H., & Fu, Z. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00651.2011 · Cited by 13
“DRF greatly shifted the circadian phases of clock genes in the heart of type 2 diabetic rats within 5 days, which is consistent with the well-known fact that DRF can entrain most peripheral clocks not only in the normal rodents (9, 16, 35, 37, 41) but also in type 1 diabetic mice (24) within several days.”
Impact of Time-Restricted Feeding to Late Night on Adaptation to a 6 h Phase Advance of the Light-Dark Cycle in Mice
Ren, B., Ma, C., Chen, L., FitzGerald, G. A., & Yang, G. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.634187 · Cited by 14
Diet-altered body temperature rhythms are associated with altered rhythms of clock gene expression in peripheral tissues in vivo
Goh, G. H., Mark, P. J., Blache, D., Binks, D., Parsons, R., Rawashdeh, O., & Maloney, S. K. (2021) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2021.102983 · Cited by 13
The effects of lighting conditions and food restriction paradigms on locomotor activity of common spiny mice, Acomys cahirinus
Chabot, C. C., Connolly, D. M., & Waring, B. B. (2012) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-10-6 · Cited by 13
“In other nocturnal species, diurnal bouts of daytime activity has been shown to entrain a variety of tissues to the daily RF schedule [32-35].”
Background
Serotonin suppresses food anticipatory activity and synchronizes the food-entrainable oscillator during time-restricted feeding
Rozenblit‐Susan, S., Chapnik, N., Genzer, Y., & Froy, O. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.019 · Cited by 13
Daily Rhythm of Lactate Dehydrogenase in Rat (Rattus norvegicus) Carrying a Per1-luciferase Transgene: Assessment on Serum and Liver
Costa, A. S. H., Castañón‐Cervantes, O., Menaker, M., Piccione, G. G., & CAOLA, G. (2005) · Veterinary Research Communications · doi:10.1007/s11259-005-0038-9 · Cited by 13
“feeding) (D´ iaz-Muˇ noz et al., 2000; Hara et al., 2001; Stokkan et al., 2001).”
Background
Misaligned feeding schedule elicits divergent circadian reorganizations in endo- and exocrine pancreas clocks
Honzlová, P., Novosadová, Z., Houdek, P., Sládek, M., & Sumová, A. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04354-7 · Cited by 12
“The response in the liver was in accordance with our previous data [8, 30] as well as data from others [7, 32, 33] and served us here as proof of concept confirming that 10 days of the misaligned feeding schedule was sufficient to affect metabolic functions and peripheral clocks.”
Result
Multiomics analyses reveal dynamic bioenergetic pathways and functional remodeling of the heart during intermittent fasting
Arumugam, T. V., Shaik, A. A., Liehn, E. A., Selvaraji, S., Poh, L., Rajeev, V., Cho, Y., Cho, Y. E., Kim, J.-H., Kim, J., et al. (2023) · eLife · doi:10.7554/elife.89214 · Cited by 27
Food anticipatory circadian rhythms in mice entrained to long or short day photoperiods
Power, S. C., & Mistlberger, R. E. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112939 · Cited by 12
Protocol for setup and circadian analysis of inverted feeding in mice
Xin, H., Huang, R., Zhou, M., Bao, X., Chen, J., Zeng, F., Wan, X., Tong, S., Deng, F., Li, M., et al. (2021) · STAR Protocols · doi:10.1016/j.xpro.2021.100701 · Cited by 12
“CRITICAL: When performing time-restricted feeding under 12 h light:12 h dark cycles, the 7-day regimen is normally applied and sufficient to entrain the liver clock (Damiola et al., 2000; Stokkan et al., 2001; Hara et al., 2001).”
Method
Time-restricted feeding alters the efficiency of mammary tumor growth
Walker, W. H., Kaper, A. L., Meléndez‐Fernández, O. H., Bumgarner, J. R., Liu, J. A., Walton, J. C., DeVries, A. C., & Nelson, R. J. (2021) · Chronobiology International · doi:10.1080/07420528.2021.2011306 · Cited by 12
“Time-restricted feeding mice can shift clock gene expression within the liver and gastrointestinal track independent of the SCN (Hara et al. 2001; Hoogerwerf et al. 2007).”
BackgroundInfluential
Induction of internal circadian desynchrony by misaligning zeitgebers
Heyde, I., & Oster, H. (2022) · Scientific Reports · doi:10.1038/s41598-022-05624-x · Cited by 12

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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