A Balanced Diet Is Necessary for Proper Entrainment Signals of the Mouse Liver Clock
Open accessAbstract
BACKGROUND: The peripheral circadian clock in mice is entrained not only by light-dark cycles but also by daily restricted feeding schedules. Behavioral and cell culture experiments suggest an increase in glucose level as a factor in such feeding-induced entrainment. For application of feeding-induced entrainment in humans, nutrient content and dietary variations should be considered. PRINCIPAL FINDING: To elucidate the food composition necessary for dietary entrainment, we examined whether complete or partial substitution of dietary nutrients affected phase shifts in liver clocks of mice. Compared with fasting mice or ad libitum fed mice, the liver bioluminescence rhythm advanced by 3-4 h on the middle day in Per2::luciferase knock-in mice that were administered a standard mouse diet, i.e. AIN-93M formula [0.6-0.85 g/10 g mouse BW] (composition: 14% casein, 47% cornstarch, 15% gelatinized cornstarch, 10% sugar, 4% soybean oil, and 10% other [fiber, vitamins, minerals, etc.]), for 2 days. When each nutrient was tested alone (100% nutrient), an insignificant weak phase advance was found to be induced by cornstarch and soybean oil, but almost no phase advance was induced by gelatinized cornstarch, high-amylose cornstarch, glucose, sucrose, or casein. A combination of glucose and casein without oil, vitamin, or fiber caused a significant phase advance. When cornstarch in AIN-93M was substituted with glucose, sucrose, fructose, polydextrose, high-amylose cornstarch, or gelatinized cornstarch, the amplitude of phase advance paralleled the increase in blood glucose concentration. CONCLUSIONS: Our results strongly suggest the following: (1) balanced diets containing carbohydrates/sugars and proteins are good for restricted feeding-induced entrainment of the peripheral circadian clock and (2) a balanced diet that increases blood glucose, but not by sugar alone, is suitable for entrainment. These findings may assist in the development of dietary recommendations for on-board meals served to air travelers and shift workers to reduce jet lag-like symptoms.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [267]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000) · Genes & Development · doi:10.1101/gad.183500 · Cited by 2,394 · see citing works
Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329 · see citing works
Stephan, F. K., & Zucker, I. (1972) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.69.6.1583 · Cited by 2,039 · see citing works
Resetting central and peripheral circadian oscillators in transgenic rats
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R.-I., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., & Tei, H. (2000) · Science · doi:10.1126/science.288.5466.682 · Cited by 1,907 · see citing works
Entrainment of the circadian clock in the liver by feeding
Stokkan, K.-A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001) · Science · doi:10.1126/science.291.5503.490 · Cited by 1,800 · see citing works
Circadian food-anticipatory activity: Formal models and physiological mechanisms
Mistlberger, R. E. (1994) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)90023-x · Cited by 857 · see citing works
Circadian rhythms in isolated brain regions
Abe, M., Herzog, E. D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., & Block, G. D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00350.2002 · Cited by 681 · see citing works
The “other” circadian system: food as a Zeitgeber
Stephan, F. K. (2002) · Journal of Biological Rhythms · doi:10.1177/074873002129002591 · Cited by 672 · see citing works
Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus
Hara, R., Wan, K., Wakamatsu, H., Aida, R., Moriya, T., Akiyama, M., & Shibata, S. (2001) · Genes to Cells · doi:10.1046/j.1365-2443.2001.00419.x · Cited by 569 · cited 3× · see citing works
“According to a standard protocol for restricted feeding [12], AIM-93M tablets were freely given to mice during a period of 4 h (ZT6-ZT10) for 14 days (14-day group).”
BackgroundMethodMolecular Genetics of Circadian Rhythms in Mammals
King, D. P., & Takahashi, J. S. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.713 · Cited by 551 · see citing works
Glucocorticoid hormones inhibit food‐induced phase‐shifting of peripheral circadian oscillators
Minh, N. L., Damiola, F., Tronche, F., Schütz, G., & Schibler, U. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7128 · Cited by 467 · see citing works
Role of neuropeptides in appetite regulation and obesity – A review
Arora, S., & Anubhuti, A. (2006) · Neuropeptides · doi:10.1016/j.npep.2006.07.001 · Cited by 451 · see citing works
Food availability and daily biological rhythms.
Boulos, Z., & Terman, M. (1980) · Neuroscience and Biobehavioral Reviews · doi:10.1016/0149-7634(80)90010-x · Cited by 367 · see citing works
Hirota, T., Okano, T., Kokame, K., Shirotani-Ikejima, H., Miyata, T., & Fukada, Y. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206233200 · Cited by 317 · see citing works
Wakamatsu, H., Yoshinobu, Y., Aida, R., Moriya, T., Akiyama, M., & Shibata, S. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01483.x · Cited by 308 · see citing works
Self-citationRice: a high or low glycemic index food?
Miller, J., Pang, E., & Bramall, L. (1992) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/56.6.1034 · Cited by 302 · see citing works
Lack of Food Anticipation in Per2 Mutant Mice
Feillet, C. A., Ripperger, J. A., Magnone, M. C., Dulloo, A. G., Albrecht, U., & Challet, É. (2006) · Current Biology · doi:10.1016/j.cub.2006.08.053 · Cited by 208 · see citing works
Is the food‐entrainable circadian oscillator in the digestive system?
Davidson, A. J., Poole, A. S., Yamazaki, S., & Menaker, M. (2003) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2003.00005.x · Cited by 180 · see citing works
Dietary Fiber and Resistant Starch
Englyst, H. N., & Kingman, S. M. (1990) · Springer eBooks · doi:10.1007/978-1-4613-0519-4_4 · Cited by 178 · see citing works
Cholecystokinin and gut–brain signalling
Dockray, G. J. (2009) · Regulatory Peptides · doi:10.1016/j.regpep.2009.03.015 · Cited by 168 · see citing works
Alterations of the Circadian Clock in the Heart by Streptozotocin-induced Diabetes
Young, M. E., Wilson, C. R., Razeghi, P., Guthrie, P. H., & Taegtmeyer, H. (2002) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2001.1504 · Cited by 165 · see citing works
Dietary fiber and resistant starch
Englyst, H. N., Trowell, H. C., Southgate, D. A., et al. (1987) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/46.6.873 · Cited by 134 · see citing works
Glucose, but not fat, phase shifts the feeding-entrained circadian clock
Stephan, F. K., & Davidson, A. J. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00166-8 · Cited by 93 · see citing works
Meerlo, P., van den Hoofdakker, R. H., Koolhaas, J. M., & Daan, S. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200109 · Cited by 86 · see citing works
Effects of Preparation Time on Phase of Cultured Tissues Reveal Complexity of Circadian Organization
Yoshikawa, T., Yamazaki, S., & Menaker, M. (2005) · Journal of Biological Rhythms · doi:10.1177/0748730405280775 · Cited by 83 · see citing works
The relevance of the glycaemic index to our understanding of dietary carbohydrates
Frost, G. S., & Dornhorst, A. (2000) · Diabetic Medicine · doi:10.1046/j.1464-5491.2000.00266.x · Cited by 82 · see citing works
Plasma secretin, CCK, and pancreatic secretion in response to dietary fat in the rat
Green, G. M., Taguchi, S., Friestman, J., et al. (1989) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1989.256.6.g1016 · Cited by 79 · see citing works
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 · see citing works
Calories Affect Zeitgeber Properties of the Feeding Entrained Circadian Oscillator
Stephan, F. K. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00204-7 · Cited by 65 · see citing works
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 · see citing works
Effect of feeding on peripheral circadian rhythms and behaviour in mammals
Kobayashi, H., Oishi, K., Hanai, S., & Ishida, N. (2004) · Genes to Cells · doi:10.1111/j.1365-2443.2004.00769.x · Cited by 62 · see citing works
Krieger, D. T. (1972) · Science · doi:10.1126/science.178.4066.1205 · Cited by 61 · see citing works
Hayasaka, N., Yaita, T., Kuwaki, T., Honma, S., Honma, K., Kudo, T., & Shibata, S. (2007) · Endocrinology · doi:10.1210/en.2007-0010 · Cited by 43 · see citing works
Self-citationBechtold, D. A. (2008) · Journal of Genetics · doi:10.1007/s12041-008-0067-6 · Cited by 42 · see citing works
Cholecystokinin‐A receptors regulate photic input pathways to the circadian clock
Shimazoe, T., Morita, M., Ogiwara, S., et al. (2007) · The FASEB Journal · doi:10.1096/fj.07-9372com · Cited by 21 · see citing works
Parenteral feeding abolishes the circadian adrenocortical rhythm in rats
Saito, M., Kato, H., Suda, M., et al. (1981) · Cellular and Molecular Life Sciences · doi:10.1007/bf01967962 · Cited by 14 · see citing works
Diurnal and seasonal variation of cholecystokinin peptides in humans
Lundberg, K., Josefsson, A., & Nordin, C. (2007) · Neuropeptides · doi:10.1016/j.npep.2006.09.049 · Cited by 13 · see citing works
Attenuated blood corticosterone rhythm in rats with jejunal resection
Kato, H., Saito, M., & Shimazu, T. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90620-9 · Cited by 9 · see citing works
Liu, X., Ogawa, H., Kishida, T., & Ebihara, K. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2008.10.007 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [39]Moriya T Aida R Kudo T Akiyama M Doi M 2009 Differential effect of acute feeding and restricted feeding on clock gene expression in mouse. Eur J Neurosci. in press
Cited by
Sorted by citations
Tahara, Y., & Shibata, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.049 · Cited by 198 · see citing works
Self-citationNutrients, Clock Genes, and Chrononutrition
Oike, H., Oishi, K., & Kobori, M. (2014) · Current Nutrition Reports · doi:10.1007/s13668-014-0082-6 · Cited by 198 · see citing works
Papakonstantinou, E., Oikonomou, C., Nychas, G., & Dimitriadis, G. D. (2022) · Nutrients · doi:10.3390/nu14040823 · Cited by 199 · see citing works
Sato-Mito, N., Sasaki, S., Murakami, K., Okubo, H., Takahashi, Y., Shibata, S., Yamada, K., & Sato, K. (2011) · Sleep Medicine · doi:10.1016/j.sleep.2010.09.012 · Cited by 191 · see citing works
Self-citationPhysiological responses to food intake throughout the day
Johnston, J. D. (2014) · Nutrition Research Reviews · doi:10.1017/s0954422414000055 · Cited by 158 · see citing works
Heaton, L. E., Davis, J. K., Rawson, E. S., Nuccio, R. P., Witard, O. C., Stein, K. W., Baar, K., Carter, J. M., & Baker, L. B. (2017) · Sports Medicine · doi:10.1007/s40279-017-0759-2 · Cited by 158 · see citing works
Meal frequency patterns determine the phase of mouse peripheral circadian clocks
Kuroda, H., Tahara, Y., Saito, K., Ohnishi, N., Kubo, Y., Seo, Y., Otsuka, M., Fuse, Y., Ohura, Y., Hirao, A., et al. (2012) · Scientific Reports · doi:10.1038/srep00711 · Cited by 105 · see citing works
Self-citationChrono-biology, Chrono-pharmacology and Chrono-nutrition
Tahara, Y., & Shibata, S. (2014) · Journal of Pharmacological Sciences · doi:10.1254/jphs.13r06cr · Cited by 94 · see citing works
Self-citationHirao, A., Nagahama, H., Tsuboi, T., Hirao, M., Tahara, Y., & Shibata, S. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00330.2010 · Cited by 86 · see citing works
- Authors
- Hirao, A., Tahara, Y., Kimura, I., & Shibata, S.
- Affiliations
- Waseda University (JP)
- Corresponding author
- Shibata, Shigenobu
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-09-07
- Volume
- 4
- Issue
- 9
- Pages
- e6909
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2734168
- OpenAlex
- W2051815114
- Cited by
- 98
- References
- 39
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2023: 8 · 2022: 6 · 2021: 7 · 2020: 2 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 6 · 2015: 10 · 2014: 9 · 2013: 6 · 2012: 8
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Japan Society for the Promotion of Science (20390065, 19659058)
- 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
- peripheral circadian clock, liver clock, phase shift, blood glucose, corn starch, casein, soybean oil, high-amylose maize starch, glucose, sucrose, fructose, polydextrose, jet lag, shift work, meal timing
- MeSH terms
- Animals, Animal Feed, Behavior, Animal, Blood Glucose, Caseins, Circadian Rhythm, Glucose, Liver, Male, Mice, Inbred C57BL, Mice, Transgenic, Models, Biological, Time Factors, Vitamins, Mice, Period Circadian Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
