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Effects of Light and Food Schedules on Liver and Tumor Molecular Clocks in Mice
Open accessAbstract
BACKGROUND: Disrupted circadian coordination accelerates malignant growth, but the molecular mechanism is unclear. METHODS: Healthy or Glasgow osteosarcoma-bearing mice (n = 162) were synchronized with light and darkness over 2-3 weeks, submitted to an 8-hour advance onset of light every 2 days (chronic jet lag) to disrupt circadian coordination, or submitted to chronic jet lag and meal timing to prevent molecular clock alteration. The expression of molecular clock genes and of the cell cycle genes c-Myc and p53 in liver and tumor was determined with quantitative reverse transcription-polymerase chain reaction at six circadian times over a 24-hour period of light and darkness and analyzed with analysis of variance and cosinor. Tumor weight was measured daily over the course of the experiment. All statistical tests were two-sided. RESULTS: In synchronized mice, mean mRNA levels of clock genes Rev-erbalpha, Per2, and Bmal1 varied by 206-, four-, and 26-fold, respectively, over the 24 hours in healthy mouse liver; by 36-, 35-, and 32-fold in the livers of tumor-bearing mice; and by 9.4-, 5.5-, and sixfold in tumor tissue (P = .046 to <.001). In mice subjected to chronic jet lag, the periodic changes were dampened and the clock gene rhythms were temporally shifted in liver and ablated in tumor, and tumor growth was accelerated. Meal timing reversed the chronic jet lag-induced alterations in Rev-erbalpha and Per2 expression in liver and of all three clock genes in tumor and slowed tumor growth. Tumor growth differed as a function of light and feeding schedules (P = .04). No obvious rhythm was detected for p53 or c-Myc in liver or tumor tissues of synchronized mice. In healthy mice subjected to chronic jet lag, the mean level of p53 expression was cut in half (P = .002), and a 12-fold circadian variation in c-Myc mRNA level (P = .03) was induced in the liver of healthy mice, whereas complex expression patterns were found in the liver and tumor of tumor-bearing mice. CONCLUSIONS: Altered light-dark or feeding schedules modified the expression of molecular clock genes and genes involved in carcinogenesis and tumor progression.
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“this protocol has been shown to disrupt the oscillations of the core circadian genes in multiple tissues (Filipski et al., 2005; Lee et al., 2010; Thaiss et al., 2014).”
From Circadian Rhythm Disruption Promotes Lung Tumorigenesis (2016) · cites this paper as Filipski et al., 2005
In the citing paper
“Emerging evidence in several different cellular and in vivo models points to an important role of the core circadian genes in carcinogenesis (Filipski et al., 2005; Fu et al., 2002; Gery et al., 2006; Janich et al., 2011; Kettner et al., 2014; Lee et al., 2010; Puram et al., 2016; Sahar and Sassone-Corsi, 2009; Van Dycke et al., 2015; Wood et al., 2008).”
From Circadian Rhythm Disruption Promotes Lung Tumorigenesis (2016) · cites this paper as Filipski et al., 2005
In the citing paper
“Earlier reports using germline mutations in circadian components have highlighted a role for circadian rhythm disruption in tumor predisposition (Filipski et al., 2005; Fu et al., 2002; Gery et al., 2006; Janich et al., 2011; Kettner et al., 2014; Lee et al., 2010; Sahar and Sassone-Corsi, 2009; Van Dycke et al., 2015; Wood et al., 2008).”
From Circadian Rhythm Disruption Promotes Lung Tumorigenesis (2016) · cites this paper as Filipski et al., 2005
In the citing paper
“This would be in line with other studies in which phase advances induce c-myc expression directly and 3 days after exposure [11, 27”
From Chronically Alternating Light Cycles Increase Breast Cancer Risk in Mice (2015) · cites this paper as [11]
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Clairambault, J., Michel, P., & Benoît Perthame, B. (2007) · Birkhäuser Boston eBooks · doi:10.1007/978-0-8176-4558-8_21 · Cited by 15
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“Indeed, tumor growth is enhanced by perturbations of the central hypothalamic clock [11]–[ 13 ] and this is most likely related to cell cycle control disruption [14], [15].”
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BackgroundHealthy Diet and Reduction of Chronic Disease Risks of Night Shift Workers
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“Controlling for circadian effects: There is also strong evidence that daily circadian rhythms can affect responses to treatments (Filipski et al. 1999; Granda et al. 2001; Filipski et al. 2002; Granda and Levi 2002; Mormont and Levi 2003; Filipski et al. 2004; Filipski et al. 2005; Granda et al. 2005; Li et al. 2005;…”
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Clairambault, J. (2006) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2006.260855 · Cited by 11
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“Syn-chrony in peak and trough core clock gene expression times between the SCN and organs is not perfect; notably, feeding time may also serve as an entrainment cue, causing circadian phase advances or delays in organs such as the liver, depending upon the feeding schedule (11 – 13).”
BackgroundCircadian Regulation of Hormesis for Health and Longevity
Jagota, A., Thummadi, N. B., & Kukkemane, K. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814253-0.00020-6 · Cited by 9
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“Deregulation of the expression of c-Myc is believed to constitute a major pathogenetic mechanism in the establishment of the cancer-prone phenotype of Per2-mutant mice, and a risk factor for tumour growth in wildtype mice with disrupted circadian cycle.[38,58] As the mechanisms of induction of DNA repair and apoptosis…”
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Lévi, F. (2008) · IEEE Engineering in Medicine and Biology Magazine · doi:10.1109/memb.2007.907361 · Cited by 7
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Self-citationOutdoor light at night and risk of liver cancer in the NIH-AARP diet and health study
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“Mice that are chronically jet-lagged by altered light–dark cycles have significantly reduced expression of clock genes and modified expression of genes involved in carcinogenesis and liver tumor progression [5].”
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“The chronobiological approach within the remedy of cancer has been recognized in rodents and humans (Filipski et al. 2005).”
BackgroundTime of Day-Dependent Responses to Cisplatin Treatment in a Male Mouse Model of Hepatoma
Akyel, Y. K., Selby, C. P., Sancar, A., & Abdo, A. N. (2025) · Journal of Biological Rhythms · doi:10.1177/07487304251349893 · Cited by 4
“Rhythmicity among tissues is influenced by signals from the suprachiasmatic nucleus, the “master clock,” as well as other factors such as feeding (Filipski et al., 2005; Mange et al., 2017; Weger et al., 2021).”
When Clocks Go Rogue: Circadian Rhythms and the Rise of Cancer
Robinson, A. S., Bennett, S. E., & Sato, S. (2026) · Journal of Biological Rhythms · doi:10.1177/07487304251391270 · Cited by 4
“Nevertheless, experimental studies in rodents support a causal link between circadian disruption and accelerated cancer progression and metastasis (Hadadi et al., 2020; Papagiannakopoulos et al., 2016; Lawther et al., 2022; Filipski and Lévi, 2009; Filipski et al., 2004, 2005; Lee et al., 2010).”
Diet and Circadian Rhythms: Implications for Aging and Longevity
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“The SCN generates circadian physiology through diffusible signals, including transforming growth factor , epidermal growth factor (EGF), prokineticin-2 (PK-2), cardiotrophin-like cytokine, and neuroanatomic sympathetic and parasympathetic pathways (Levi et al. 2010; Dibner et al. 2010 ).”
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“…activity, endocrine system, body temperature, hepatic metabolism, etc. (Panda et al. 2002; Weaver 2002) Disruption of these circadian clocks that drive these rhythms favors cancer processes and reduces survival in cancerous rodents and human patients (Filipski et al. 2005; Innominato et al. 2009).”
BackgroundPathophysiology, Associations and Consequences of Circadian Rhythm Sleep Disorders
Youngstedt, S. D., & Burch, J. B. (2008) · CRC Press eBooks · doi:10.3109/9781420019926-13 · Cited by 3
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Relevance of Circadian Rhythm in Cancer
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“Under a jet lag paradigm, in which mice with tumor xenografts were subject to repeated 8 h light shifts, the rate of tumor growth also increased, with a mitigation of the effect occurring when meal time was matched to the light shifts; food-derived cues are dominant peripheral entraining signals, which reinforce the p…”
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Metadata
- Authors
- Filipski, E., Innominato, P. F., Wu, M., Li, X.-M., Iacobelli, S., Xian, L.-J., & Levi, F.
- Affiliations
- Inserm (FR)
- Corresponding author
- Filipski, E.
- Venue
- JNCI Journal of the National Cancer Institute
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-04-05
- Volume
- 97
- Issue
- 7
- Pages
- 507-517
- ISSN
- 0027-8874 (ISSN-L)
- 1460-2105
- OpenAlex
- W2128032039
- Cited by
- 200
- References
- 48
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 6 · 2022: 6 · 2021: 7 · 2020: 10 · 2019: 6 · 2018: 10 · 2017: 9 · 2016: 14 · 2015: 9 · 2014: 13 · 2013: 12 · 2012: 12
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- JNCI Journal of the National Cancer Institute (publishedVersion)
- PubMed (publishedVersion)
- INFM-OAR (INFN Catania) (submittedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (other-oa)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Health Sciences › Medicine › Physiology (medical) › Dietary Effects on Health
- Keywords
- circadian rhythm, jet lag, light-dark cycle, meal timing, feeding schedule, clock genes, NR1D1, Per2, Bmal1, osteosarcoma, liver, tumor growth, p53, c-Myc, carcinogenesis, tumor progression, molecular clock
- MeSH terms
- Analysis of Variance, Animals, Circadian Rhythm, DNA-Binding Proteins, Food, Light, Liver, Male, Nuclear Proteins, RNA, Messenger, Transcription Factors, Gene Expression Regulation, Neoplastic, Tumor Suppressor Protein p53, Proto-Oncogene Proteins c-myc, Receptors, Cytoplasmic and Nuclear, Cell Cycle Proteins, Reverse Transcriptase Polymerase Chain Reaction, Mice, Period Circadian Proteins, Nuclear Receptor Subfamily 1, Group D, Member 1
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