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Circadian Disruption in Experimental Cancer Processes
Open accessAbstract
The circadian timing system (CTS) coordinated by the suprachiasmatic nuclei (SCN) of the hypothalamus regulates daily rhythms of behavior, physiology, as well as cellular metabolism and proliferation. Altered circadian rhythms predict for poor survival in cancer patients. An increased incidence of several cancers has been reported in flight attendants and in shift workers. To explore the contribution of the CTS to tumor growth, we developed experimental models of disrupted or enhanced circadian coordination through stereotaxic destruction of the SCN, modifications of photoperiodic or feeding synchronizers and/or the administration of pharmacologic agents. SCN ablation or exposure to experimental chronic jetlag (CJL, consisting of an 8-hour advance of the light-dark cycle every 2 days) caused alterations in circadian physiology and significantly accelerated tumor growth. CJL suppressed or altered the rhythms of clock gene and cell cycle gene expression in mouse liver. It increased p53 and decreased c-Myc expression, a result in line with the promotion of diethylnitrosamine -initiated hepatocarcinogenesis in jet-lagged mice. The accelerating effect of CJL on tumor growth was counterbalanced by the regular timing of food access over the 24-h. Meal timing prevented the circadian disruption produced by CJL and slowed down tumor growth. In synchronized mice, meal timing reinforced host circadian coordination, phase-shifted the transcriptional rhythms of clock genes in the liver of tumor-bearing mice and slowed down cancer progression. These results support the role of the CTS in cancer progression and call for the development of therapeutic strategies aimed at preventing or treating circadian clock dysfunctions.
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Hu, L., Harper, A. S., Heer, E. V., McNeil, J., Cao, C., Park, Y., Martell, K., Gotto, G. T., Shen‐Tu, G., Peters, C., et al. (2020) · Cancers · doi:10.3390/cancers12123873 · Cited by 17
“Such discrepancies generate a profound influence on the temporal alignment of genetic and metabolic processes [36].”
BackgroundRhythm 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
Impaired light detection of the circadian clock in a zebrafish melanoma model
Hamilton, N., Diaz-de-Cerio, N., & Whitmore, D. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1014146 · Cited by 17
“Mice, whose clock had been surgically disrupted by removal of the suprachiasmatic nucleus, and then inoculated with tumor cells showed an increase in tumourigenesis.(13) Environmental clock disruptions by constant light or jet lag exposure in rats and mice have also revealed an increase in spontaneous tumor appearance…”
BackgroundMolina‐Aguilar, C., Guerrero-Carrillo, M. D. J., Espinosa-Aguirre, J. J., Olguín-Reyes, S. D. R., Castro-Belio, T., Martínez, O. V., Rivera-Zavala, J. B., & Díaz‐Muñoz, M. (2017) · Carcinogenesis · doi:10.1093/carcin/bgx052 · Cited by 16
Circadian system and aging: where both times interact
Cobarro, C., Soares, L. I., Kutsenko, Y., & Tomás‐Loba, A. (2025) · Frontiers in Aging · doi:10.3389/fragi.2025.1646794 · Cited by 15
“Also, rodents subjected to jetlag conditions exhibited accelerated tumor growth, increased metastasis, and impaired antitumor immune responses (Filipski and Lévi, 2009; Roberts et al., 2022).”
Brain activity and transcriptional profiling in mice under chronic jet lag
Gao, Q., Khan, S., & Zhang, L. (2020) · Scientific Data · doi:10.1038/s41597-020-00709-6 · Cited by 13
Circadian rhythms disruption in cancer
Lopes‐Júnior, L. C., & Veronez, L. C. (2021) · Biological Rhythm Research · doi:10.1080/09291016.2021.1951470 · Cited by 15
Ayan, D., & Ak, Ç. (2023) · Hepatology forum/Hepatology forum (Online) · doi:10.14744/hf.2023.2023.0009 · Cited by 12
“[30,31] Analysis of miRNA profiles in liver from Clock gene mutant mice reveals that Clock gene-regulated miRNAs may play a role in cancer initiation or progression by controlling genes involved in cell proliferation, invasion, and/or metabolism in mouse liver.”
Dibner, C., Sadowski, S. M., Triponez, F., & Philippé, J. (2017) · Biomarkers in Medicine · doi:10.2217/bmm-2016-0316 · Cited by 13
Zhao, N., Tang, Yang, K., & Chen, D. (2013) · OncoTargets and Therapy · doi:10.2147/ott.s39955 · Cited by 12
“Circadian rhythms affect tissues and cells through neurotransmitters and endocrine regulation, controlling all levels of life processes, such as activity, rest, metabolism, cell proliferation, endocrine function, and immune responses, in a coordinated and timely ordered manner.(7,11) Therefore,”
BackgroundTime to fight: targeting the circadian clock molecular machinery in cancer therapy
Astone, M., & Santoro, M. M. (2021) · Drug Discovery Today · doi:10.1016/j.drudis.2021.01.023 · Cited by 10
Circadian rhythms measured by actigraphy during oncological treatments: a systematic review
Huang, C., Madsen, M. T., & Gögenür, I. (2015) · Biological Rhythm Research · doi:10.1080/09291016.2015.1004840 · Cited by 10
“The idea of using locomotor rest-activity to characterize circadian rhythm was derived from animal studies, where SCN abolishment, chronic jet lag exposure, or external de-synchronization led to suppression of this rest-activity rhythm (Filipski & Levi 2009).”
MethodLa cronodisrupción como causa de envejecimiento
Ortiz‐Tudela, E., Bonmatí‐Carrión, M., la Fuente, M. D., & Mendiola, P. (2011) · Revista Española de Geriatría y Gerontología · doi:10.1016/j.regg.2011.09.013 · Cited by 15
Herichová, I. (2024) · Biomedical Journal · doi:10.1016/j.bj.2024.100784 · Cited by 9
“Long-term circadian deregulation can promote or worsen several pathologies, including cancer [4,5].”
Zhang, Z., Gao, W., Tan, X., Deng, T., Zhou, W., Jian, H., & Zeng, P. (2023) · BMC Cancer · doi:10.1186/s12885-023-10508-y · Cited by 9
“Moreover, growing evidence supports that disfunction of circadian clock genes is common and may promotes liver carcinogenesis and accelerated cancer progression [11, 13].”
BackgroundThe role of neural-related factors in the metastasis of the gastrointestinal cancer
Zeng, H., Xu, X., Xu, B., & Song, Q. (2013) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.122505 · Cited by 9
Characterization of locomotor activity circadian rhythms in athymic nude mice
Paladino, N., Duhart, J. M., Fedele, M. L. M., & Golombek, D. A. (2013) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-11-2 · Cited by 9
“Given the increasing interest in the effects of circadian disruption on cancer biology [20-25] and the extended use of athymic mice as an useful tool for cancer studies, we aimed to characterize the circadian rhythms in nude and their corresponding control strain mice (Swiss Webster).”
MethodRajan, P. K., Udoh, U. S., Finley, R., Pierre, S. V., & Sanabria, J. R. (2024) · Biomedicines · doi:10.3390/biomedicines12091961 · Cited by 8
“In mice, DEN was also reported to disrupt circadian rhythms of rest activity and body temperature [148,149].”
BackgroundDeziel, N. C., Wang, R., Warren, J. L., Dinauer, C., Ogilvie, J. B., Clark, C. J., Zhong, C., Wiemels, J. L., Morimoto, L. M., Metayer, C., et al. (2025) · Environmental Health Perspectives · doi:10.1289/ehp14849 · Cited by 9
Melatonin and Circadian Rhythm: Aging, Cancer, and Mechanism
Kovacic, P., & Somanathan, R. (2014) · Open Journal of Preventive Medicine · doi:10.4236/ojpm.2014.47065 · Cited by 8
“The circadian timing system coordinated by the suprachiasmatic nuclei (SCN) of the hypothalamus regulates daily rhythms of behavior, physiology, as well as cellular metabolism and proliferation [47].”
BackgroundModeling and analysis of the impacts of jet lag on circadian rhythm and its role in tumor growth
Hassan, A., Ahmad, J., Ashraf, H., & Ali, A. (2018) · PeerJ · doi:10.7717/peerj.4877 · Cited by 8
Critical Effects on Akt Signaling in Adult Zebrafish Brain Following Alterations in Light Exposure
Moore, N., Mans, R. A., McCauley, M. K., Allgood, C. S., & Barksdale, K. A. (2021) · Cells · doi:10.3390/cells10030637 · Cited by 8
“models [1,2,41,54]) and alterations in GSK3β, Akt, and HSP70 are examined in the brains of adult zebrafish via exposure to four days of altered, unpredictable light exposure”
BackgroundMethodSultan, A. (2018) · Biological Rhythm Research · doi:10.1080/09291016.2018.1498197 · Cited by 8
“…shift work, social jetlag, and irregular food intake) and genetic, has been broadly implicated in various pathologies (Figure 4a) such as cancer (Filipski and Lévi 2009; Papagiannakopoulos et al. 2016; Sultan et al. 2014, Sultan et al. 2017b, 2017c, 2017d), cardiovascular disease (Morris et al.…”
BackgroundCo, M. T.-H., & Kwong, A. (2020) · Clinical Breast Cancer · doi:10.1016/j.clbc.2020.05.003 · Cited by 8
The Importance of Timing in Immunotherapy: A Systematic Review
Nagy, S. S., Hussein, A. M., & Kesselman, M. M. (2025) · Cureus · doi:10.7759/cureus.82994 · Cited by 7
“Animal models have shown that ablation of the suprachiasmatic nucleus or chronic jet lag in humans has led to elevated tumor growth and progression levels due to creating a beneficial microenvironment for tumor growth [14,17,18].”
Sleep disorders in hepatocellular carcinoma
Qian, J., Ruan, M., Wang, Z., Dong, W., Jia, J.-H., Feng, X.-C., & Liu, H. (2025) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v17.i10.110503 · Cited by 5
“…between the endogenous circadian clock and environmental light-dark cycles, caused by factors like shift work or transmeridian travel, disrupts organismal homeostasis (including sleep-wake patterns, metabolic processes, and hormone secretion), thereby increasing carcinogenic risk[21,22].”
The role of circadian and redox rhythms in cancer hypoxia
Omer, S., Karunagaran, D., & Suraishkumar, G. K. (2021) · Advances in Redox Research · doi:10.1016/j.arres.2021.100018 · Cited by 6
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).”
Effect of chronic jet lag after induction of Dalton's lymphoma in male and female mice
Basu, P., Tripathi, R., Mishra, R., & Singaravel, M. (2011) · Biological Rhythm Research · doi:10.1080/09291016.2011.579756 · Cited by 4
“As a result, survival is much lower in clinical and experimental subjects with cancer, who are also subjected to some form of circadian rhythm disruption (Filipski et al. 2004; Filipski and Lévi 2009).”
BackgroundBasu, P., & Singaravel, M. (2013) · Biological Rhythm Research · doi:10.1080/09291016.2013.770294 · Cited by 3
“Maladjustment to abruptly altered light–dark schedules causes a plethora of problems including cognitive deficits (Gibson et al. 2010), metabolic disturbances (Karatsoreos et al. 2011), cancer (Filipski & Levi 2009) and mortality (Davidson et al. 2006; Basu, Tripathi et al. 2012).”
BackgroundEXPRESSION OF CLOCK GENE IN COLORECTAL CANCER PATIENTS IS DEPENDENT ON TUMOR LOCATION
Hasakova, K., Vician, M., Reis, R. D. F., Zeman, M., & Herichová, I. (2018) · Pathophysiology · doi:10.1016/j.pathophys.2018.07.144 · Cited by 3
Hong-bing, G., & Liang, C. Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.725024 · Cited by 3
“CCRN4L, a type of clock-control gene, is a key component in the regulation of circadian rhythms (Filipski and Lévi, 2009).”
BackgroundLes hôtesses de l’air sont-elles à risque accru de cancer du sein ?
Gassmann, A.-S., Gonzalez, M., & Mathelin, C. (2014) · Gynécologie Obstétrique & Fertilité · doi:10.1016/j.gyobfe.2014.09.008 · Cited by 3
Metadata
- Authors
- Filipski, E., & Lévi, F.
- Affiliations
- Université Paris-Sud (FR)
- Hôpital Paul Brousse, Villejuif, France, Université Paris-Sud, Orsay, France
- Corresponding author
- Filipski, Elisabeth
- Venue
- Integrative Cancer Therapies
- Publisher
- SAGE Publications
- Published
- 2009-12
- Volume
- 8
- Issue
- 4
- Pages
- 298-302
- ISSN
- 1534-7354 (ISSN-L)
- 1552-695X
- OpenAlex
- W2036196597
- Cited by
- 125
- References
- 38
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 9 · 2023: 3 · 2022: 7 · 2021: 10 · 2020: 7 · 2019: 5 · 2018: 8 · 2017: 7 · 2016: 4 · 2015: 10 · 2014: 13 · 2013: 15 · 2012: 8
- FWCI
- 2.69
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Integrative Cancer Therapies (publishedVersion)
- PubMed (publishedVersion)
- 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 › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- circadian rhythm, circadian clock, suprachiasmatic nucleus, circadian rhythm disruption, tumor growth, jet lag, meal timing, photoperiod, clock genes, p53, c-Myc, hepatocarcinogenesis, diethylnitrosamine, liver cancer, shift work, tumor progression
- MeSH terms
- Animals, Chronic Disease, Circadian Rhythm, Disease Models, Animal, Food, Male, Neoplasms, Experimental, Suprachiasmatic Nucleus, Photoperiod, Disease Progression, Jet Lag Syndrome, Mice
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