Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus
Open accessAbstract
In mammals, circadian oscillators exist not only in the suprachiasmatic nucleus, which harbors the central pacemaker, but also in most peripheral tissues. It is believed that the SCN clock entrains the phase of peripheral clocks via chemical cues, such as rhythmically secreted hormones. Here we show that temporal feeding restriction under light–dark or dark–dark conditions can change the phase of circadian gene expression in peripheral cell types by up to 12 h while leaving the phase of cyclic gene expression in the SCN unaffected. Hence, changes in metabolism can lead to an uncoupling of peripheral oscillators from the central pacemaker. Sudden large changes in feeding time, similar to abrupt changes in the photoperiod, reset the phase of rhythmic gene expression gradually and are thus likely to act through a clock-dependent mechanism. Food-induced phase resetting proceeds faster in liver than in kidney, heart, or pancreas, but after 1 wk of daytime feeding, the phases of circadian gene expression are similar in all examined peripheral tissues.
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Food intake during the biological night can uncouple peripheral clocks from the SCN.
“However, food intake during the biological night can uncouple peripheral clocks from the SCN (31, 32), confirming that meal timing acts as a zeitgeber for circadian clocks.”
From Meal timing and its role in obesity and associated diseases (2024) · cites this paper as [32]
The paper’s “Daytime feeding uncouples peripheral circadian oscillators from the central SCN pacemaker” section says the opposite of the attributed timing: in nocturnal mice, daytime feeding uncoupled peripheral clocks from the SCN, whereas nighttime feeding had little effect on circadian gene-expression phase. The abstract likewise identifies feeding during the subjective day—not the biological night—as producing uncoupling. (LLM, conf=0.91)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredIn 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 [262]
Exogenous behavioral time cues associated with externally imposed schedules have the capacity to drive endogenous rhythmicity in metabolism, likely by impacting peripheral oscillators and dissociating them from the rhythm of the central SCN pacemaker.
“Exogenous, behavioral time cues associated with externally imposed schedules thus have the capacity to drive endogenous rhythmicity in metabolism, likely by impacting on peripheral oscillators (17, 18) and dissociating them from the rhythm of the central SCN pacemaker.”
From Separation of circadian- and behavior-driven metabolite rhythms in humans provides a window on peripheral oscillators and metabolism (2018) · cites this paper as [17]
The feeding/fasting cycle is the main Zeitgeber for synchronization of peripheral clocks.
“A few years later it became clear that the feeding/fasting cycle is the main Zeitgeber in terms of the synchronization of these so-called peripheral clocks [6].”
From Circadian control of glucose metabolism (2014) · cites this paper as [6]
In animals, timed feeding is a strong resetting cue for peripheral clocks.
“In animals, timed feeding is a strong resetting cue for peripheral clocks (51,52).”
From Role of the circadian system in cardiovascular disease (2018) · cites this paper as [51]
Feeding rodents only during the rest phase can phase shift peripheral oscillators in the liver, pancreas, kidney, and heart while having no effect on the phase of the SCN.
“Feeding rodents only during the rest phase—as similarly occurs during night work when they eat during their night shift—can phase shift peripheral oscillators in the liver, pancreas, kidney, and heart while it has no effect on the phase of the SCN (Damiola et al., 2000; Stokkan et al., 2001).”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Damiola et al., 2000
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- Authors
- Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U.
- Affiliations
- University of Geneva (CH)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2000-12-01
- Volume
- 14
- Issue
- 23
- Pages
- 2950-2961
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC317100
- OpenAlex
- W2164628441
- Cited by
- 2,394
- References
- 62
- Citations by year
- 2026: 78 · 2025: 116 · 2024: 112 · 2023: 98 · 2022: 125 · 2021: 129 · 2020: 146 · 2019: 111 · 2018: 124 · 2017: 108 · 2016: 112 · 2015: 116 · 2014: 102 · 2013: 103 · 2012: 97
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Louis-Jeantet Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (47314)
- Bonizzi-Theler Stiftung
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- circadian clock, feed restriction, suprachiasmatic nucleus, peripheral circadian oscillators, phase resetting, circadian gene expression, photoperiod, liver, kidney, heart, pancreas
- MeSH terms
- Animals, Aryl Hydrocarbon Hydroxylases, Biological Clocks, Body Temperature, Circadian Rhythm, Cytochrome P-450 Enzyme System, DNA-Binding Proteins, Eye Proteins, Feeding Behavior, Flavoproteins, Food, Food Deprivation, Mixed Function Oxygenases, Kinetics, Liver, Neurons, Nuclear Proteins, Proteins, Suprachiasmatic Nucleus, Transcription Factors, Photoreceptor Cells, Invertebrate, Receptors, Cytoplasmic and Nuclear, Cell Cycle Proteins, Drosophila Proteins, Receptors, G-Protein-Coupled, Mice, Cryptochromes, Period Circadian Proteins, Nuclear Receptor Subfamily 1, Group D, Member 1, Cytochrome P-450 CYP2A6
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