Dysregulation of inflammatory responses by chronic circadian disruption
Open accessAbstract
Circadian rhythms modulate nearly every mammalian physiological process. Chronic disruption of circadian timing in shift work or during chronic jet lag in animal models leads to a higher risk of several pathologies. Many of these conditions in both shift workers and experimental models share the common risk factor of inflammation. In this study, we show that experimentally induced circadian disruption altered innate immune responses. Endotoxemic shock induced by LPS was magnified, leading to hypothermia and death after four consecutive weekly 6-h phase advances of the light/dark schedule, with 89% mortality compared with 21% in unshifted control mice. This may be due to a heightened release of proinflammatory cytokines in response to LPS treatment in shifted animals. Isolated peritoneal macrophages harvested from shifted mice exhibited a similarly heightened response to LPS in vitro, indicating that these cells are a target for jet lag. Sleep deprivation and stress are known to alter immune function and are potential mediators of the effects we describe. However, polysomnographic recording in mice exposed to the shifting schedule revealed no sleep loss, and stress measures were not altered in shifted mice. In contrast, we observed altered or abolished rhythms in the expression of clock genes in the central clock, liver, thymus, and peritoneal macrophages in mice after chronic jet lag. We conclude that circadian disruption, but not sleep loss or stress, are associated with jet lag-related dysregulation of the innate immune system. Such immune changes might be a common mechanism for the myriad negative health effects of shift work.
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In shift-work or chronic jet-lag animal models, long-term circadian disruption amplifies inflammatory reactions to endotoxin.
“the chronic disruption of circadian rhythm magnifies inflammatory responses to challenge with endotoxin in an animal model of shift work or chronic jet lag (Castanon-Cervantes et al, 2010)”
From Sleep health: Reciprocal regulation of sleep and innate immunity (2017) · cites this paper as Castanon-Cervantes et al, 2010
The risk of death following the in vivo LPS challenge was significantly greater in shifted than control mice.
“Furthermore, the risk of death following the in vivo LPS challenge was significantly greater in the shifted than control mice.”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Castanon-Cervantes et al., 2010
Twenty-four hours after a lipopolysaccharide (LPS) challenge, systemic concentrations of proinflammatory cytokines IL-1β, GM-CSF, IL-12, and IL-13 were significantly higher in shifted than control mice.
“Twenty-four hours after a lipopolysaccharide (LPS) challenge, systemic concentrations of the proinflammatory cytokines interleukine-1β (IL-1β), granulocyte macrophage colony-stimulating factor, IL-12, and IL-13 were significantly higher in the shifted than control mice.”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Castanon-Cervantes et al., 2010
The circadian phase angle at the time of the LPS challenge was similar between shifted and control animals, and therefore the findings were not due to the stimulus being given at a different circadian time.
“The circadian phase angle, as assessed by body temperature; locomotor activity; and Per2 expression in four tissues (SCN, liver, thymus, and spleen), at the time of the LPS challenge was similar between the shifted and control animals, and therefore the findings were not due to the stimulus being given at a different circadian time between the two groups.”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Castanon-Cervantes et al., 2010
Increased IL-6 release in shifted mice was also observed during in vitro LPS stimulation of macrophages.
“The increased IL-6 release in the shifted mice was also observed during in vitro LPS stimulation of macrophages.”
From The impact of the circadian timing system on cardiovascular and metabolic function (2012) · cites this paper as Castanon-Cervantes et al., 2010
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Mechanisms linking circadian clocks, sleep, and neurodegeneration
Musiek, E. S., & Holtzman, D. M. (2016) · Science · doi:10.1126/science.aah4968 · Cited by 878 · see citing works
Circadian misalignment increases cardiovascular disease risk factors in humans
Morris, C. J., Purvis, T. E., Hu, K., & Scheer, F. A. J. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516953113 · Cited by 691 · see citing works
Sleep health: Reciprocal regulation of sleep and innate immunity
Irwin, M. R., & Opp, M. R. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.148 · Cited by 624 · see citing works
Redox regulation of SIRT1 in inflammation and cellular senescence
Hwang, J.-W., Yao, H., Caito, S., Sundar, I. K., & Rahman, I. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.03.015 · Cited by 503 · see citing works
The circadian clock and pathology of the ageing brain
Kondratova, A. A., & Kondratov, R. V. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3208 · Cited by 482 · see citing works
Circadian disruption and human health
Fishbein, A. B., Knutson, K. L., & Zee, P. C. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148286 · Cited by 468 · see citing works
Crucian, B. E., Choukèr, A., Simpson, R. J., Mehta, S., Marshall, G., Smith, S. M., Zwart, S. R., Heer, M., Ponomarev, S., Whitmire, A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01437 · Cited by 421 · see citing works
Circadian rhythms, time-restricted feeding, and healthy aging
Manoogian, E. N. C., & Panda, S. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.12.006 · Cited by 330 · see citing works
Health Consequences of Circadian Disruption in Humans and Animal Models
Evans, J. A., & Davidson, A. J. (2013) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-396971-2.00010-5 · Cited by 291 · see citing works
Self-citationCrosstalk between the circadian clock circuitry and the immune system
Cermakian, N., Lange, T., Golombek, D., Sarkar, D., Nakao, A., Shibata, S., & Mazzoccoli, G. (2013) · Chronobiology International · doi:10.3109/07420528.2013.782315 · Cited by 279 · see citing works
Circadian rhythm and the gut microbiome
Voigt, R. M., Forsyth, C. B., Green, S. J., Engen, P. A., & Keshavarzian, A. (2016) · International Review of Neurobiology · doi:10.1016/bs.irn.2016.07.002 · Cited by 274 · see citing works
The impact of the circadian timing system on cardiovascular and metabolic function
Morris, C. J., Yang, J. N., & Scheer, F. A. J. L. (2012) · Progress in Brain Research · doi:10.1016/b978-0-444-59427-3.00019-8 · Cited by 215 · see citing works
Tahara, Y., & Shibata, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.049 · Cited by 198 · see citing works
Endocrine Effects of Circadian Disruption
Bedrosian, T. A., Fonken, L. K., & Nelson, R. J. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105102 · Cited by 170 · see citing works
Immune System: An Emerging Player in Mediating Effects of Endocrine Disruptors on Metabolic Health
Bansal, A., Henao-Mejia, J., & Simmons, R. A. (2018) · Endocrinology · doi:10.1210/en.2017-00882 · Cited by 152 · see citing works
McCarthy, M. J., Gottlieb, J. F., Gonzalez, R., McClung, C. A., Alloy, L. B., Cain, S., Dulcis, D., Etain, B., Frey, B. N., Garbazza, C., et al. (2022) · Bipolar Disorders · doi:10.1111/bdi.13165 · Cited by 136 · see citing works
Mammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Alibhai, F. J., Tsimakouridze, E. V., Chinnappareddy, N., Wright, D. C., Billia, F., O’Sullivan, M. L., Pyle, W. G., Sole, M. J., & Martino, T. A. (2014) · Circulation Research · doi:10.1161/circresaha.114.302995 · Cited by 122 · see citing works
Sleep Loss and Cytokines Levels in an Experimental Model of Psoriasis
Hirotsu, C., Rydlewski, M., Araújo, M. S., Tufik, S., & Andersen, M. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051183 · Cited by 103 · see citing works
Foundations of circadian medicine
Kramer, A., Lange, T., Spies, C., Finger, A.-M., Berg, D., & Oster, H. (2022) · PLOS Biology · doi:10.1371/journal.pbio.3001567 · Cited by 99 · see citing works
“Exposing mice to a chronodisruptive environment such as repeated shifts in the light–dark cycle (simulating shift work or jetlag) increases mortality in aged animals [29], promotes tumor growth [30] and autoimmune processes [31], and dysregulates inflammatory responses [32].”
BackgroundChrono-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
Chen, S., Fuller, K. K., Dunlap, J. C., & Loros, J. J. (2018) · Journal of Biological Rhythms · doi:10.1177/0748730417745178 · Cited by 15 · see citing works
“This has important implications in human health, particularly for shift-workers, whose circadian disruption leads to dysregulation of the immune system, heightening the risk of various immunopathologies, including those associated with pathogen encounter (Castanon-Cervantes et al., 2010).”
Sleep Medicine - Asleep or Awake?
(2024) · doi:10.5772/intechopen.104201 · Cited by 5 · see citing works
- Authors
- Castanon-Cervantes, O., Wu, M., Ehlen, J. C., Paul, K., Gamble, K. L., Johnson, R. L., Besing, R. C., Menaker, M., Gewirtz, A. T., & Davidson, A. J.
- Affiliations
- Neuroscience Institute, Morehouse School of Medicine , Atlanta, GA 30310
- Morehouse School of Medicine (US)
- University of Alabama at Birmingham (US)
- University of Virginia (US)
- Emory University (US)
- Corresponding author
- Wu, Mingwei
- Paul, Ketema
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-11
- Volume
- 185
- Issue
- 10
- Pages
- 5796-5805
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC2974025
- OpenAlex
- W2140832481
- Cited by
- 542
- References
- 87
- Citations by year
- 2026: 20 · 2025: 38 · 2024: 33 · 2023: 28 · 2022: 29 · 2021: 57 · 2020: 50 · 2019: 29 · 2018: 31 · 2017: 42 · 2016: 38 · 2015: 27 · 2014: 28 · 2013: 48 · 2012: 23
- FWCI
- 13.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Morehouse School of Medicine
- National Cancer Institute (P20CA132389)
- National Institute of General Medical Sciences (GM086683, R00GM086683, K99GM086683)
- National Institute of Neurological Disorders and Stroke (U54NS060659, 5U54NS-060659-020001)
- National Center for Research Resources (G12RR03034, G12RR003034)
- National Institute on Minority Health and Health Disparities (S21MD000101)
- 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 › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- circadian rhythm disruption, jet lag, shift work, innate immunity, endotoxic shock, lipopolysaccharide, inflammatory cytokines, peritoneal macrophages, clock genes, hypothermia, immune dysregulation
- MeSH terms
- Animals, Biological Clocks, Circadian Rhythm, Enzyme-Linked Immunosorbent Assay, Inflammation, Mice, Inbred C57BL, Cytokines, Polysomnography, Macrophages, Peritoneal, Reverse Transcriptase Polymerase Chain Reaction, Jet Lag Syndrome, Gene Expression Profiling, Mice, Gene Knock-In Techniques
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.
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