Combination of starvation interval and food volume determines the phase of liver circadian rhythm in Per2::Luc knock-in mice under two meals per day feeding

Hirao, Akiko; Nagahama, Hiroki; Tsuboi, Takuma; Hirao, Mizuho; Tahara, Yu; Shibata, Shigenobu

doi:10.1152/ajpgi.00330.2010

Cited by 86Circadian rhythm and melatoninDietary Effects on HealthRegulation of Appetite and Obesity

Combination of starvation interval and food volume determines the phase of liver circadian rhythm in Per2::Luc knock-in mice under two meals per day feeding

Hirao, Akiko, Nagahama, Hiroki, Tsuboi, Takuma, Hirao, Mizuho, Tahara, Yu, Shibata, Shigenobu·2010·American Journal of Physiology-Gastrointestinal and Liver Physiology

DOI 10.1152/ajpgi.00330.2010

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Abstract

Although the circadian liver clock is entrained by the feeding cycle, factors such as food volume and starvation interval are poorly understood. Per2::Luc knock-in mice were given two meals per day with different food volume sizes and/or with different intervals of starvation between two mealtimes with the total food volume per day fixed at 3.6 g (80 food pellets, ∼75% of free feeding) per mouse. The bioluminescence rhythm in the liver produced a unimodal peak but not bimodal peak under the regimen of two meals per day over 14-15 days. Peak Per2 expression occurred concurrently with the mealtime of the larger food volume, when the first and second meal were given as different food volume ratios under a 12 h feeding interval. When an equal volume of food was given under different starvation interval (8 h:16 h), the peak of the Per2 rhythm was close to peak by mealtime after long starvation (16 h). When food volumes for each mealtime were changed under 8 h:16 h, the peak rhythm was influenced by combined factors of food volume and starvation interval. Food intake after the 16-h starvation caused a significant increase in liver Per2, Dec1, and Bmal1 gene expression compared with food intake after the 8-h starvation with 8 h:16 h feeding intervals. In conclusion, the present results clearly demonstrate that food-induced entrainment of the liver clock is dependent on both food volume and the starvation interval between two meals. Therefore, normal feeding habits may help to maintain normal clock function in the liver organ.

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The liver clock is affected by the balance between food intake and starvation intervals.
“The liver clock is affected by the balance between food intake and starvation intervals [267,268,269].”
From Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance (2022) · cites this paper as [269]

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Itokawa, M., Hirao, A., Nagahama, H., Otsuka, M., Ohtsu, T., Furutani, N., Hirao, K., Hatta, T., & Shibata, S. (2013) · Nutrition Research · doi:10.1016/j.nutres.2012.12.004 · Cited by 41 · see citing works
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Delayed Timing of Eating: Impact on Weight and Metabolism
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Breakfast consumption pattern and its association with overweight and obesity among university students: a population-based study
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Background
Feeding and adrenal entrainment stimuli are both necessary for normal circadian oscillation of peripheral clocks in mice housed under different photoperiods
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“Feeding after a long fast (e.g. breakfast) caused strong entrainment of peripheral clocks (Hirao et al., 2010; Kuroda et al., 2012), whereas feeding 4 or 6 meals per day at equal intervals failed to produce entrainment (Kuroda et al., 2012).”
Background
Phase shifts in circadian peripheral clocks caused by exercise are dependent on the feeding schedule in PER2::LUC mice
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Night eating model shows time-specific depression-like behavior in the forced swimming test
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“We chose these measures of meal timing because the first intake of the day has been implicated in setting the phase of circadian clocks(6,7), and the midpoint of the daily intake window indicates whether consumption habits are typically centred around an earlier or a later time in the day.”
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Entrainment of mouse peripheral circadian clocks to <24 h feeding/fasting cycles under 24 h light/dark conditions
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l-Ornithine affects peripheral clock gene expression in mice
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“The consumed food volume and the starvation intervals between the meals are able to alter the liver clock (Hirao et al., 2010) and restricted feeding can even rapidly uncouple the liver rhythm from that of SCN (Stokkan et al.”
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Association of Eating Pattern, Chronotype, and Social Jetlag: A Cross-Sectional Study Using Data Accumulated in a Japanese Food-Logging Mobile Health Application
Nitta, L., Tahara, Y., Shinto, T., Makino, S., Kuwahara, M., Tada, A., Abe, N., Michie, M., & Shibata, S. (2023) · Nutrients · doi:10.3390/nu15092165 · Cited by 17 · see citing works
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Caffeine suppresses high-fat diet-induced body weight gain in mice depending on feeding timing
Haraguchi, A., Yamazaki, T., Ryan, C., Ito, K., Sato, S., Tamura, K., Sekiguchi, M., Cao, S., & Shibata, S. (2022) · Journal of Functional Foods · doi:10.1016/j.jff.2022.105307 · Cited by 15 · see citing works
2,2,2-Tribromoethanol Phase-Shifts the Circadian Rhythm of the Liver Clock in Per2::Luciferase Knockin Mice: Lack of Dependence on Anesthetic Activity
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“For example, presentation of restricted feeding stimuli for 1 to 4 days during the daytime produces a phase advance of the liver clock, with a dependence on the restricted feeding days (Hirao et al., 2010).”
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The impact of an implementation intention to improve mealtimes and reduce jet lag in long-haul cabin crew
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“Further, they also provide support for the role of dietary change in improving jet lag (e.g. Reynolds & Montgomery, 2002; Schoeller et al., 1997) and the role of mealtimes in resetting the body clock (Hirao et al., 2010).”
BackgroundResult
A low-protein diet eliminates the circadian rhythm of serum insulin and hepatic lipid metabolism in mice
Yokota, S.-I., Nakamura, K., Ando, M., Haraguchi, A., Omori, K., & Shibata, S. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.10.004 · Cited by 13 · see citing works
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Short-term daytime restricted feeding in rats with high salt impairs diurnal variation of Na+excretion
Rhoads, M. K., Speed, J. S., Roth, K. J., Zhang, D., Jin, C., Gamble, K. L., & Pollock, D. M. (2022) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00287.2021 · Cited by 8 · see citing works
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Longitudinal associations of skipping breakfast and night eating with 4-year changes in weight and waist circumference among Chinese adults
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“In future experiments, refeeding should be done near ZT12 and/or the peripheral clock should be measured after several cycles of a two meal per day schedule (Hirao et al. 2010).”
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Exenatide administration time-dependently affects the hepatic circadian clock through glucagon-like peptide-1 receptors in the central nervous system
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Authors: Hirao, A., Nagahama, H., Tsuboi, T., Hirao, M., Tahara, Y., & Shibata, S.
Affiliations: Waseda University (JP)
Corresponding author: Shibata, Shigenobu
ORCID: Tahara, Yu
Shibata, Shigenobu
Venue: American Journal of Physiology-Gastrointestinal and Liver Physiology
Publisher: American Physiological Society
Published: 2010-11
Volume: 299
Issue: 5
Pages: G1045-G1053
ISSN: 0193-1857 (ISSN-L)
1522-1547
DOI: 10.1152/ajpgi.00330.2010
OpenAlex: W2114822868
Semantic Scholar: 1915c8bc27118cca83927114fd5e26ccc6a6f0a8
Cited by: 86
References: 41
Citations by year: 2026: 3 · 2025: 3 · 2024: 6 · 2023: 4 · 2022: 6 · 2021: 6 · 2020: 2 · 2019: 8 · 2018: 8 · 2017: 3 · 2016: 6 · 2015: 4 · 2014: 9 · 2013: 6 · 2012: 8
FWCI: 2.60
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Health Sciences › Medicine › Physiology › Dietary Effects on Health
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: food volume, DEC1, Bmal1, mealtime
MeSH terms: Analysis of Variance, Animals, Biological Clocks, Body Weight, Circadian Rhythm, Eating, Feeding Behavior, Liver, Male, Mice, Transgenic, Starvation, Reverse Transcriptase Polymerase Chain Reaction, Mice, Period Circadian Proteins

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Combination of starvation interval and food volume determines the phase of liver circadian rhythm in Per2::Luc knock-in mice under two meals per day feeding

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