Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T17:26:56.307Z Has data issue: false hasContentIssue false

12 - Disrupted Circadian Rhythms and Immune Function

Published online by Cambridge University Press:  07 October 2023

By
Louise M. Ince ,
Devin Simpkins  and
Julie E. Gibbs
Edited by
Laura K. Fonken  and
Randy J. Nelson
Laura K. Fonken
Affiliation:
University of Texas, Austin
Randy J. Nelson
Affiliation:
West Virginia University
Get access

Summary

The immune system is a highly dynamic element of physiology, sensitive to both the external environment and organism-intrinsic factors. Inflammatory responses of sufficient magnitude are required to maintain homeostasis and protect from disease, but must be resolved on an appropriate timescale to prevent excessive damage and chronic inflammation. The circadian clock is a critical regulator of immune function and circadian disruption is a known risk factor in multiple diseases, disturbing physiological processes and exacerbating inflammation. Interactions between the circadian clock and immune system are bidirectional, as pathogens and inflammatory molecules can themselves disrupt local rhythms in cells and tissues. Here, we discuss the evidence linking circadian disruption with maladaptive immune function, including studies of shift work, sleep deficiency, genetic disruption of rhythms, and animal models of inflammatory diseases.

Keywords

inflammationshift worksleepcytokinesinnate immunityadaptive immunity
Type
Chapter
Information
Biological Implications of Circadian Disruption
A Modern Health Challenge
 , pp. 256 - 284
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acevedo, N., Saaf, A., Soderhall, C., Melen, E., Mandelin, J., Pietras, C. O., Ezer, S., Karisola, P., Vendelin, J., Gennas, G. B., Yli-Kauhaluoma, J., Alenius, H., von Mutius, E., Doekes, G., Braun-Fahrlander, C., Riedler, J., van Hage, M., D’Amato, M., Scheynius, A., … Pulkkinen, V. (2013). Interaction between retinoid acid receptor-related orphan receptor alpha (RORA) and neuropeptide S receptor 1 (NPSR1) in asthma. PLoS One, 8(4), e60111.CrossRefGoogle Scholar
Amir, M., Chaudhari, S., Wang, R., Campbell, S., Mosure, S. A., Chopp, L. B., Lu, Q., Shang, J., Pelletier, O. B., He, Y., Doebelin, C., Cameron, M. D., Kojetin, D. J., Kamenecka, T. M., & Solt, L. A. (2018). REV-ERBα regulates TH17 cell development and autoimmunity. Cell Rep, 25(13), 3733–3749.e3738.Google Scholar
Atwater, A. Q., Immergluck, L. C., Davidson, A. J., & Castanon-Cervantes, O. (2021). Shift work predicts increases in lipopolysaccharide-binding protein, interleukin-10, and leukocyte counts in a cross-sectional study of healthy volunteers carrying low-grade systemic inflammation. Int J Environ Res Public Health, 18(24), 13158.Google Scholar
Axelsson, J., Rehman, J. U., Akerstedt, T., Ekman, R., Miller, G. E., Hoglund, C. O., & Lekander, M. (2013). Effects of sustained sleep restriction on mitogen-stimulated cytokines, chemokines and T helper 1/T helper 2 balance in humans. PLoS One, 8(12), e82291.CrossRefGoogle Scholar
Baxter, M., & Ray, D. W. (2019). Circadian rhythms in innate immunity and stress responses. Immunology, 161(4), 261–267.CrossRefGoogle Scholar
Beurel, E., Toups, M., & Nemeroff, C. B. (2020). The bidirectional relationship of depression and inflammation: Double trouble. Neuron, 107(2), 234–256.Google Scholar
Bjorvatn, B., Axelsson, J., Pallesen, S., Waage, S., Vedaa, O., Blytt, K. M., Buchvold, H. V., Moen, B. E., & Thun, E. (2020). The association between shift work and immunological biomarkers in nurses. Front Public Health, 8, 415.CrossRefGoogle ScholarPubMed
Bonnell, E. K., Huggins, C. E., Huggins, C. T., McCaffrey, T. A., Palermo, C., & Bonham, M. P. (2017). Influences on dietary choices during day versus night shift in shift workers: A mixed methods study. Nutrients, 9(3), 193.Google Scholar
Born, J., Lange, T., Hansen, K., Molle, M., & Fehm, H. L. (1997). Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol, 158(9), 4454–4464.Google Scholar
Brown, J. P., Martin, D., Nagaria, Z., Verceles, A. C., Jobe, S. L., & Wickwire, E. M. (2020). Mental health consequences of shift work: An updated review. Curr Psychiatry Rep, 22(2), 7.Google Scholar
Buonacera, A., Stancanelli, B., Colaci, M., & Malatino, L. (2022). Neutrophil to lymphocyte ratio: An emerging marker of the relationships between the immune system and diseases. Int J Mol Sci, 23(7), 3636.Google Scholar
Calle, M. C., & Fernandez, M. L. (2012). Inflammation and type 2 diabetes. Diabetes Metab, 38(3), 183–191.Google Scholar
Canakis, A., & Qazi, T. (2020). Sleep and fatigue in IBD: An unrecognized but important extra-intestinal manifestation. Curr Gastroenterol Rep, 22(2), 8.Google Scholar
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. (2010). Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol, 185(10), 5796–5805.CrossRefGoogle ScholarPubMed
Cavadini, G., Petrzilka, S., Kohler, P., Jud, C., Tobler, I., Birchler, T., & Fontana, A. (2007). TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc Natl Acad Sci USA, 104(31), 12843–12848.Google Scholar
Chang, C., Loo, C.-S., Zhao, X., Solt, L. A., Liang, Y., Bapat, S. P., Cho, H., Kamenecka, T. M., Leblanc, M., Atkins, A. R., Yu, R. T., Downes, M., Burris, T. P., Evans, R. M., & Zheng, Y. (2019). The nuclear receptor REV-ERBα modulates Th17 cell-mediated autoimmune disease. Proc Natl Acad Sci USA, 116(37), 18528–18536.Google Scholar
Chen, M., Peng, W. Y., Tang, T. C., & Zheng, H. (2021). Differential sleep traits have no causal effect on inflammatory bowel diseases: A Mendelian randomization study. Front Pharmacol, 12, 763649.CrossRefGoogle ScholarPubMed
Chen, R., Weitzner, A. S., McKennon, L. A., & Fonken, L. K. (2021). Light at night during development in mice has modest effects on adulthood behavior and neuroimmune activation. Behav Brain Res, 405, 113171.Google Scholar
Coiffard, B., Diallo, A. B., Culver, A., Mezouar, S., Hammad, E., Vigne, C., Nicolino-Brunet, C., Dignat-George, F., Baumstarck, K., Boucekine, M., Leone, M., & Mege, J.-L. (2019). Circadian rhythm disruption and sepsis in severe trauma patients. Shock, 52(1), 29–36.CrossRefGoogle ScholarPubMed
Copertaro, A., Bracci, M., Gesuita, R., Carle, F., Amati, M., Baldassari, M., Mocchegiani, E., & Santarelli, L. (2011). Influence of shift-work on selected immune variables in nurses. Ind Health, 49(5), 597–604.Google Scholar
Crespo, M., Gonzalez-Teran, B., Nikolic, I., Mora, A., Folgueira, C., Rodriguez, E., Leiva-Vega, L., Pintor-Chocano, A., Fernandez-Chacon, M., Ruiz-Garrido, I., Cicuendez, B., Tomas-Loba, A., A-Gonzalez, N., Caballero-Molano, A., Beiroa, D., Hernandez-Cosido, L., Torres, J. L., Kennedy, N. J., Davis, R. J., … Sabio, G. (2020). Neutrophil infiltration regulates clock-gene expression to organize daily hepatic metabolism. eLife, 9, e59258.CrossRefGoogle ScholarPubMed
Cuesta, M., Boudreau, P., Dubeau-Laramee, G., Cermakian, N., & Boivin, D. B. (2016). Simulated night shift disrupts circadian rhythms of immune functions in humans. J Immunol, 196(6), 2466–2475.Google Scholar
Curtis, B. J., Ashbrook, L. H., Young, T., Finn, L. A., Fu, Y.-H., Ptáček, L. J., & Jones, C. R. (2019). Extreme morning chronotypes are often familial and not exceedingly rare: The estimated prevalence of advanced sleep phase, familial advanced sleep phase, and advanced sleep–wake phase disorder in a sleep clinic population. Sleep, 42(10), zsz148.CrossRefGoogle ScholarPubMed
Cyster, J. G., & Allen, C. D. C. (2019). B cell responses: Cell interaction dynamics and decisions. Cell, 177(3), 524–540.Google Scholar
Dinges, D. F., Douglas, S. D., Zaugg, L., Campbell, D. E., McMann, J. M., Whitehouse, W. G., Orne, E. C., Kapoor, S. C., Icaza, E., & Orne, M. T. (1994). Leukocytosis and natural killer cell function parallel neurobehavioral fatigue induced by 64 hours of sleep deprivation. J Clin Invest, 93(5), 1930–1939.Google Scholar
Downton, P., Early, J. O., & Gibbs, J. E. (2020). Circadian rhythms in adaptive immunity. Immunology, 161(4), 268–277.CrossRefGoogle ScholarPubMed
Druzd, D., Matveeva, O., Ince, L., Harrison, U., He, W., Schmal, C., Herzel, H., Tsang, A. H., Kawakami, N., Leliavski, A., Uhl, O., Yao, L., Sander, L. E., Chen, C. S., Kraus, K., de Juan, A., Hergenhan, S. M., Ehlers, M., Koletzko, B., … Scheiermann, C. (2017). Lymphocyte circadian clocks control lymph node trafficking and adaptive immune responses. Immunity, 46(1), 120–132.Google Scholar
Ebisawa, T., Uchiyama, M., Kajimura, N., Mishima, K., Kamei, Y., Katoh, M., Watanabe, T., Sekimoto, M., Shibui, K., Kim, K., Kudo, Y., Ozeki, Y., Sugishita, M., Toyoshima, R., Inoue, Y., Yamada, N., Nagase, T., Ozaki, N., Ohara, O., … Yamauchi, T. (2001). Association of structural polymorphisms in the human period3 gene with delayed sleep phase syndrome. EMBO Rep, 2(4), 342–346.Google Scholar
Edgar, R. S., Stangherlin, A., Nagy, A. D., Nicoll, M. P., Efstathiou, S., O’Neill, J. S., & Reddy, A. B. (2016). Cell autonomous regulation of herpes and influenza virus infection by the circadian clock. Proc Natl Acad Sci USA, 113(36), 10085–10090.CrossRefGoogle ScholarPubMed
Feghali, C. A., & Wright, T. M. (1997). Cytokines in acute and chronic inflammation. Front Biosci, 2, d12–d26.Google Scholar
Filipski, E., Delaunay, F., King, V. M., Wu, M. W., Claustrat, B., Grechez-Cassiau, A., Guettier, C., Hastings, M. H., & Francis, L. (2004). Effects of chronic jet lag on tumor progression in mice. Cancer Res, 64(21), 7879–7885.Google Scholar
Fondell, E., Axelsson, J., Franck, K., Ploner, A., Lekander, M., Balter, K., & Gaines, H. (2011). Short natural sleep is associated with higher T cell and lower NK cell activities. Brain Behav Immun, 25(7), 1367–1375.Google Scholar
Fonken, L. K., Aubrecht, T. G., Melendez-Fernandez, O. H., Weil, Z. M., & Nelson, R. J. (2013). Dim light at night disrupts molecular circadian rhythms and increases body weight. J Biol Rhythms, 28(4), 262–271.Google Scholar
Fonken, L. K., Bedrosian, T. A., Zhang, N., Weil, Z. M., DeVries, A. C., & Nelson, R. J. (2019). Dim light at night impairs recovery from global cerebral ischemia. Exp Neurol, 317, 100–109.Google Scholar
Fonken, L. K., Frank, M. G., Kitt, M. M., Barrientos, R. M., Watkins, L. R., & Maier, S. F. (2015). Microglia inflammatory responses are controlled by an intrinsic circadian clock. Brain Behav Immun, 45, 171–179.CrossRefGoogle ScholarPubMed
Fonken, L. K., Weil, Z. M., & Nelson, R. J. (2013). Mice exposed to dim light at night exaggerate inflammatory responses to lipopolysaccharide. Brain Behav Immun, 34, 159–163.Google Scholar
Fortier, E. E., Rooney, J., Dardente, H., Hardy, M. P., Labrecque, N., & Cermakian, N. (2011). Circadian variation of the response of T cells to antigen. J Immunol, 187(12), 6291–6300.CrossRefGoogle ScholarPubMed
Gaertner, V. D., Michel, S., Curtin, J. A., Pulkkinen, V., Acevedo, N., Söderhäll, C., von Berg, A., Bufe, A., Laub, O., Rietschel, E., Heinzmann, A., Simma, B., Vogelberg, C., Pershagen, G., Melén, E., Simpson, A., Custovic, A., Kere, J., & Kabesch, M. (2019). Nocturnal asthma is affected by genetic interactions between RORA and NPSR1. Pediat Pulmonol, 54(6), 847–857.Google Scholar
Galdiero, M. R., Marone, G., & Mantovani, A. (2018). Cancer inflammation and cytokines. Cold Spring Harb Perspect Biol, 10(8), a028662.Google Scholar
Ganeshan, K., Nikkanen, J., Man, K., Leong, Y. A., Sogawa, Y., Maschek, J. A., Van Ry, T., Chagwedera, D. N., Cox, J. E., & Chawla, A. (2019). Energetic trade-offs and hypometabolic states promote disease tolerance. Cell, 177(2), 399–413 e312.Google Scholar
Gaudet, A. D., Fonken, L. K., Ayala, M. T., Bateman, E. M., Schleicher, W. E., Smith, E. J., D’Angelo, H. M., Maier, S. F., & Watkins, L. R. (2018). Spinal cord injury in rats disrupts the circadian system. eNeuro, 5(6), ENEURO.0328-0318.2018.Google Scholar
Gibbs, J. E., Blaikley, J., Beesley, S., Matthews, L., Simpson, K. D., Boyce, S. H., Farrow, S. N., Else, K. J., Singh, D., Ray, D. W., & Loudon, A. S. (2012). The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA, 109(2), 582–587.Google Scholar
Gibbs, J. E., Ince, L., Matthews, L., Mei, J., Bell, T., Yang, N., Saer, B., Begley, N., Poolman, T., Pariollaud, M., Farrow, S. N., DeMayo, F., Hussell, T., Worthen, G. S., Ray, D. W., & Loudon, A. S. I. (2014). An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nature Med, 20(8), 919–926.Google Scholar
Golalipour, M., Maleki, Z., Farazmandfar, T., & Shahbazi, M. (2017). PER3 VNTR polymorphism in multiple sclerosis: A new insight to impact of sleep disturbances in MS. Mult Scler Relat Disord, 17, 84–86.Google Scholar
Golia, E., Limongelli, G., Natale, F., Fimiani, F., Maddaloni, V., Pariggiano, I., Bianchi, R., Crisci, M., D’Acierno, L., Giordano, R., Di Palma, G., Conte, M., Golino, P., Russo, M. G., Calabro, R., & Calabro, P. (2014). Inflammation and cardiovascular disease: From pathogenesis to therapeutic target. Curr Atheroscler Rep, 16(9), 435.Google Scholar
Guo, B., Yang, N., Borysiewicz, E., Dudek, M., Williams, J. L., Li, J., Maywood, E. S., Adamson, A., Hastings, M. H., Bateman, J. F., White, M. R., Boot-Handford, R. P., & Meng, Q. J. (2015). Catabolic cytokines disrupt the circadian clock and the expression of clock-controlled genes in cartilage via an NFκB-dependent pathway. Osteoarthritis Cartilage, 23(11), 1981–1988.Google Scholar
Halberg, F., Johnson, E. A., Brown, B. W., & Bittner, J. J. (1960). Susceptibility rhythm to E. coli endotoxin and bioassay. Proc Soc Exp Biol Med, 103, 142–144.Google Scholar
Hanprathet, N., Lertmaharit, S., Lohsoonthorn, V., Rattananupong, T., Ammaranond, P., & Jiamjarasrangsi, W. (2019). Shift work and leukocyte count changes among workers in Bangkok. Ann Work Expo Health, 63(6), 689–700.Google Scholar
He, W., Holtkamp, S., Hergenhan, S. M., Kraus, K., de Juan, A., Weber, J., Bradfield, P., Grenier, J. M. P., Pelletier, J., Druzd, D., Chen, C. S., Ince, L. M., Bierschenk, S., Pick, R., Sperandio, M., Aurrand-Lions, M., & Scheiermann, C. (2018). Circadian expression of migratory factors establishes lineage-specific signatures that guide the homing of leukocyte subsets to tissues. Immunity, 49(6), 1175–1190 e1177.Google Scholar
He, Y., Jones, C. R., Fujiki, N., Xu, Y., Guo, B., Holder, J. L. Jr., Rossner, M. J., Nishino, S., & Fu, Y.-H. (2009 ). The transcriptional repressor DEC2 regulates sleep length in mammals. Science, 325(5942), 866–870.Google Scholar
Hirano, A., Hsu, P.-K., Zhang, L., Xing, L., McMahon, T., Yamazaki, M., Ptáček Louis, J., & Fu, Y.-H. (2018). DEC2 modulates orexin expression and regulates sleep. Proc Natl Acad Sci, 115(13), 3434–3439.Google Scholar
Hirano, A., Shi, G., Jones, C. R., Lipzen, A., Pennacchio, L. A., Xu, Y., Hallows, W. C., McMahon, T., Yamazaki, M., Ptacek, L. J., & Fu, Y. H. (2016). A cryptochrome 2 mutation yields advanced sleep phase in humans. eLife, 5, e16695.Google Scholar
Hofmann, K., Clauder, A. K., & Manz, R. A. (2018). Targeting B cells and plasma cells in autoimmune diseases. Front Immunol, 9, 835.Google Scholar
Holtkamp, S. J., Ince, L. M., Barnoud, C., Schmitt, M. T., Sinturel, F., Pilorz, V., Pick, R., Jemelin, S., Muhlstadt, M., Boehncke, W. H., Weber, J., Laubender, D., Philippou-Massier, J., Chen, C. S., Holtermann, L., Vestweber, D., Sperandio, M., Schraml, B. U., Halin, C., … Scheiermann, C. (2021). Circadian clocks guide dendritic cells into skin lymphatics. Nat Immunol, 22(11), 1375–1381.Google Scholar
Hong, H. K., Maury, E., Ramsey, K. M., Perelis, M., Marcheva, B., Omura, C., Kobayashi, Y., Guttridge, D. C., Barish, G. D., & Bass, J. (2018). Requirement for NF-kappaB in maintenance of molecular and behavioral circadian rhythms in mice. Genes Dev, 32(21–22), 1367–1379.Google Scholar
Hopwood, T. W., Hall, S., Begley, N., Forman, R., Brown, S., Vonslow, R., Saer, B., Little, M. C., Murphy, E. A., Hurst, R. J., Ray, D. W., MacDonald, A. S., Brass, A., Bechtold, D. A., Gibbs, J. E., Loudon, A. S., & Else, K. J. (2018). The circadian regulator BMAL1 programmes responses to parasitic worm infection via a dendritic cell clock. Sci Rep, 8(1), 3782.Google Scholar
Hughes, A. T. L., Samuels, R. E., Bano-Otalora, B., Belle, M. D. C., Wegner, S., Guilding, C., Northeast, R. C., Loudon, A. S. I., Gigg, J., & Piggins, H. D. (2021). Timed daily exercise remodels circadian rhythms in mice. Commun Biol, 4(1), 761.Google Scholar
Hui, L., Hua, F., Diandong, H., & Hong, Y. (2007). Effects of sleep and sleep deprivation on immunoglobulins and complement in humans. Brain Behav Immun, 21(3), 308–310.Google Scholar
Hwang, J. W., Sundar, I. K., Yao, H., Sellix, M. T., & Rahman, I. (2014). Circadian clock function is disrupted by environmental tobacco/cigarette smoke, leading to lung inflammation and injury via a SIRT1-BMAL1 pathway. FASEB J, 28(1), 176–194.Google Scholar
Ibarra-Coronado, E. G., Velazquez-Moctezuma, J., Diaz, D., Becerril-Villanueva, L. E., Pavon, L., & Morales-Montor, J. (2015). Sleep deprivation induces changes in immunity in Trichinella spiralis-infected rats. Int J Biol Sci, 11(8), 901–912.Google Scholar
Inokawa, H., Umemura, Y., Shimba, A., Kawakami, E., Koike, N., Tsuchiya, Y., Ohashi, M., Minami, Y., Cui, G., Asahi, T., Ono, R., Sasawaki, Y., Konishi, E., Yoo, S.-H., Chen, Z., Teramukai, S., Ikuta, K., & Yagita, K. (2020). Chronic circadian misalignment accelerates immune senescence and abbreviates lifespan in mice. Sci Rep, 10(1), 2569.Google Scholar
Irwin, M., Mascovich, A., Gillin, J. C., Willoughby, R., Pike, J., & Smith, T. L. (1994). Partial sleep deprivation reduces natural killer cell activity in humans. Psychosom Med, 56(6), 493–498.Google Scholar
de Jager, C. P., van Wijk, P. T., Mathoera, R. B., de Jongh-Leuvenink, J., van der Poll, T., & Wever, P. C. (2010). Lymphocytopenia and neutrophil–lymphocyte count ratio predict bacteremia better than conventional infection markers in an emergency care unit. Crit Care, 14(5), R192.Google Scholar
Jaradat, M., Stapleton, C., Tilley, S. L., Dixon, D., Erikson, C. J., McCaskill, J. G., Kang, H. S., Angers, M., Liao, G., Collins, J., Grissom, S., & Jetten, A. M. (2006). Modulatory role for retinoid-related orphan receptor alpha in allergen-induced lung inflammation. Am J Respir Crit Care Med, 174(12), 1299–1309.CrossRefGoogle ScholarPubMed
Javeed, N., Brown, M. R., Rakshit, K., Her, T., Sen, S. K., & Matveyenko, A. V. (2021). Proinflammatory cytokine interleukin 1beta disrupts beta-cell circadian clock function and regulation of insulin secretion. Endocrinology, 162(1), bqaa084.Google Scholar
Jones, C. R., Campbell, S. S., Zone, S. E., Cooper, F., DeSano, A., Murphy, P. J., Jones, B., Czajkowski, L., & Ptacek, L. J. (1999). Familial advanced sleep-phase syndrome: A short-period circadian rhythm variant in humans. Nat Med, 5(9), 1062–1065.Google Scholar
Karin, M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature, 441(7092), 431–436.Google Scholar
Kervezee, L., Cuesta, M., Cermakian, N., & Boivin, D. B. (2018). Simulated night shift work induces circadian misalignment of the human peripheral blood mononuclear cell transcriptome. Proc Natl Acad Sci USA, 115(21), 5540–5545.Google Scholar
Kervezee, L., Shechter, A., & Boivin, D. B. (2018). Impact of shift work on the circadian timing system and health in women. Sleep Med Clin, 13(3), 295–306.Google Scholar
Kim, S. W., Jang, E. C., Kwon, S. C., Han, W., Kang, M. S., Nam, Y. H., & Lee, Y. J. (2016). Night shift work and inflammatory markers in male workers aged 20–39 in a display manufacturing company. Ann Occup Environ Med, 28, 48.Google Scholar
Kitchen, G. B., Cunningham, P. S., Poolman, T. M., Iqbal, M., Maidstone, R., Baxter, M., Bagnall, J., Begley, N., Saer, B., Hussell, T., Matthews, L. C., Dockrell, D. H., Durrington, H. J., Gibbs, J. E., Blaikley, J. F., Loudon, A. S., & Ray, D. W. (2020). The clock gene Bmal1 inhibits macrophage motility, phagocytosis, and impairs defense against pneumonia. Proc Natl Acad Sci USA, 117(3), 1543–1551.Google Scholar
Knutsson, A., Hammar, N., & Karlsson, B. (2004). Shift workers’ mortality scrutinized. Chronobiol Int, 21(6), 1049–1053.Google Scholar
Koch, U., & Radtke, F. (2011). Mechanisms of T cell development and transformation. Annu Rev Cell Dev Biol, 27(1), 539–562.Google Scholar
Kurien, P., Hsu, P. K., Leon, J., Wu, D., McMahon, T., Shi, G., Xu, Y., Lipzen, A., Pennacchio, L. A., Jones, C. R., Fu, Y. H., & Ptacek, L. J. (2019). TIMELESS mutation alters phase responsiveness and causes advanced sleep phase. Proc Natl Acad Sci USA, 116(24), 12045–12053.Google Scholar
Lange, T., Dimitrov, S., Bollinger, T., Diekelmann, S., & Born, J. (2011). Sleep after vaccination boosts immunological memory. J Immunol, 187(1), 283–290.Google Scholar
Lange, T., Perras, B., Fehm, H. L., & Born, J. (2003). Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom Med, 65(5), 831–835.Google Scholar
Langwinski, W., Sobkowiak, P., Narozna, B., Wojsyk-Banaszak, I., Dmitrzak-Weglarz, M., Stachowiak, Z., Nowakowska, J., Breborowicz, A., & Szczepankiewicz, A. (2020). Association of circadian clock TIMELESS variants and expression with asthma risk in children. Clin Respir J, 14(12), 1191–1200.Google Scholar
Lavtar, P., Rudolf, G., Maver, A., Hodzic, A., Starcevic Cizmarevic, N., Zivkovic, M., Sega Jazbec, S., Klemenc Ketis, Z., Kapovic, M., Dincic, E., Raicevic, R., Sepcic, J., Lovrecic, L., Stankovic, A., Ristic, S., & Peterlin, B. (2018). Association of circadian rhythm genes ARNTL/BMAL1 and CLOCK with multiple sclerosis. PLoS One, 13(1), e0190601.Google Scholar
Liu, X., Yu, R., Zhu, L., Hou, X., & Zou, K. (2017). Bidirectional regulation of circadian disturbance and inflammation in inflammatory bowel disease. Inflamm Bowel Dis, 23(10), 1741–1751.Google Scholar
Loef, B., Nanlohy, N. M., Jacobi, R. H. J., van de Ven, C., Mariman, R., van der Beek, A. J., Proper, K. I., & van Baarle, D. (2019). Immunological effects of shift work in healthcare workers. Sci Rep, 9(1), 18220.Google Scholar
Logan, R. W., Zhang, C., Murugan, S., O’Connell, S., Levitt, D., Rosenwasser, A. M., & Sarkar, D. K. (2012). Chronic shift-lag alters the circadian clock of NK cells and promotes lung cancer growth in rats. J Immunol, 188(6), 2583–2591.Google Scholar
Long, J. E., Drayson, M. T., Taylor, A. E., Toellner, K. M., Lord, J. M., & Phillips, A. C. (2016). Morning vaccination enhances antibody response over afternoon vaccination: A cluster-randomised trial. Vaccine, 34(24), 2679–2685.Google Scholar
Lu, Z., Klein-Cardeña, K., Lee, S., Antonsen, T. M., Girvan, M., & Ott, E. (2016). Resynchronization of circadian oscillators and the east-west asymmetry of jet-lag. Chaos: An Interdisciplinary J Nonlinear Sci, 26(9), 094811.Google Scholar
Maidstone, R. J., Turner, J., Vetter, C., Dashti, H. S., Saxena, R., Scheer, F., Shea, S. A., Kyle, S. D., Lawlor, D. A., Loudon, A. S. I., Blaikley, J. F., Rutter, M. K., Ray, D. W., & Durrington, H. J. (2021). Night shift work is associated with an increased risk of asthma. Thorax, 76(1), 53–60.Google Scholar
van Mark, A., Weiler, S. W., Schroder, M., Otto, A., Jauch-Chara, K., Groneberg, D. A., Spallek, M., Kessel, R., & Kalsdorf, B. (2010). The impact of shift work induced chronic circadian disruption on IL-6 and TNF-alpha immune responses. J Occup Med Toxicol, 5(1), 18.Google Scholar
Mazzoccoli, G., Palmieri, O., Corritore, G., Latiano, T., Bossa, F., Scimeca, D., Biscaglia, G., Valvano, M. R., D’Inca, R., Cucchiara, S., Stronati, L., Annese, V., Andriulli, A., & Latiano, A. (2012). Association study of a polymorphism in clock gene PERIOD3 and risk of inflammatory bowel disease. Chronobiol Int, 29(8), 994–1003.Google Scholar
McNeely, E., Mordukhovich, I., Staffa, S., Tideman, S., Gale, S., & Coull, B. (2018). Cancer prevalence among flight attendants compared to the general population. Environ Health, 17(1), 49.Google Scholar
McNeely, E., Mordukhovich, I., Tideman, S., Gale, S., & Coull, B. (2018). Estimating the health consequences of flight attendant work: comparing flight attendant health to the general population in a cross-sectional study. BMC Public Health, 18(1), 346.Google Scholar
Medzhitov, R. (2008). Origin and physiological roles of inflammation. Nature, 454(7203), 428–435.Google Scholar
Meier, D., Lopez, M., Franken, P., & Fontana, A. (2015). Twist1 is a TNF-inducible inhibitor of clock mediated activation of period genes. PLoS One, 10(9), e0137229.Google Scholar
Micic, G., Lovato, N., Gradisar, M., Ferguson, S. A., Burgess, H. J., & Lack, L. C. (2016). The etiology of delayed sleep phase disorder. Sleep Med Rev, 27, 29–38.Google Scholar
Moffatt, M. F., Gut, I. G., Demenais, F., Strachan, D. P., Bouzigon, E., Heath, S., von Mutius, E., Farrall, M., Lathrop, M., Cookson, W., & GABRIEL Consortium (2010). A large-scale, consortium-based genomewide association study of asthma. N Engl J Med, 363(13), 1211–1221.Google Scholar
Mohren, D. C., Jansen, N. W., Kant, I. J., Galama, J., van den Brandt, P. A., & Swaen, G. M. (2002). Prevalence of common infections among employees in different work schedules. J Occup Environ Med, 44(11), 1003–1011.Google Scholar
Monk, T. H., Buysse, D. J., Carrier, J., & Kupfer, D. J. (2000). Inducing jet-lag in older people: Directional asymmetry. J Sleep Res, 9(2), 101–116.CrossRefGoogle ScholarPubMed
Nagai, M., Morikawa, Y., Kitaoka, K., Nakamura, K., Sakurai, M., Nishijo, M., Hamazaki, Y., Maruzeni, S., & Nakagawa, H. (2011). Effects of fatigue on immune function in nurses performing shift work. J Occup Health, 53(5), 312–319.Google Scholar
Nobis, C. C., Laramée, G. D., Kervezee, L., de Sousa, D. M., Labrecque, N., & Cermakian, N. (2019). The circadian clock of CD8 T cells modulates their early response to vaccination and the rhythmicity of related signaling pathways. Proc Natl Acad Sci USA, 116(40), 20077–20086.Google Scholar
Oliva-Ramirez, J., Moreno-Altamirano, M. M., Pineda-Olvera, B., Cauich-Sanchez, P., & Sanchez-Garcia, F. J. (2014). Crosstalk between circadian rhythmicity, mitochondrial dynamics and macrophage bactericidal activity. Immunology, 143(3), 490–497.Google Scholar
Pariollaud, M., Gibbs, J., Hopwood, T., Brown, S., Begley, N., Vonslow, R., Poolman, T., Guo, B., Saer, B., Jones, D. H., Tellam, J. P., Bresciani, S., Tomkinson, N. C. O., Wojno-Picon, J., Cooper, A. W. J., Daniels, D. A., Trump, R. P., Grant, D., Zuercher, W., … Ray, D. W. (2018). Circadian clock component REV-ERBα controls homeostatic regulation of pulmonary inflammation. J Clin Invest, 128(6), 2281–2296.Google Scholar
Patke, A., Murphy, P. J., Onat, O. E., Krieger, A. C., Ozcelik, T., Campbell, S. S., & Young, M. W. (2017). Mutation of the human circadian clock gene CRY1 in familial delayed sleep phase disorder. Cell, 169(2), 203–215 e213.Google Scholar
Pearson, G. L., Savenkova, M., Barnwell, J. J., & Karatsoreos, I. N. (2020). Circadian desynchronization alters metabolic and immune responses following lipopolysaccharide inoculation in male mice. Brain Behav Immun, 88, 220–229.Google Scholar
Pellegrino, R., Kavakli, I. H., Goel, N., Cardinale, C. J., Dinges, D. F., Kuna, S. T., Maislin, G., Van Dongen, H. P. A., Tufik, S., Hogenesch, J. B., Hakonarson, H., & Pack, A. I. (2014). A novel BHLHE41 variant is associated with short sleep and resistance to sleep deprivation in humans. Sleep, 37(8), 1327–1336.Google Scholar
Pennock, N. D., White, J. T., Cross, E. W., Cheney, E. E., Tamburini, B. A., & Kedl, R. M. (2013). T cell responses: Naive to memory and everything in between. Adv Physiol Educ, 37(4), 273–283.Google Scholar
Prather, A. A., Hall, M., Fury, J. M., Ross, D. C., Muldoon, M. F., Cohen, S., & Marsland, A. L. (2012). Sleep and antibody response to hepatitis B vaccination. Sleep, 35(8), 1063–1069.Google Scholar
Prather, A. A., Janicki-Deverts, D., Hall, M. H., & Cohen, S. (2015). Behaviorally assessed sleep and susceptibility to the common cold. Sleep, 38(9), 1353–1359.Google Scholar
Puttonen, S., Harma, M., & Hublin, C. (2010). Shift work and cardiovascular disease: Pathways from circadian stress to morbidity. Scand J Work Environ Health, 36(2), 96–108.Google Scholar
Puttonen, S., Oksanen, T., Vahtera, J., Pentti, J., Virtanen, M., Salo, P., & Kivimaki, M. (2010). Is shift work a risk factor for rheumatoid arthritis? The Finnish Public Sector study. Ann Rheum Dis, 69(4), 779–780.Google Scholar
Puttonen, S., Viitasalo, K., & Harma, M. (2011). Effect of shiftwork on systemic markers of inflammation. Chronobiol Int, 28(6), 528–535.Google Scholar
Reinhardt, E. L., Fernandes, P., Markus, R. P., & Fischer, F. M. (2019). Night work effects on salivary cytokines TNF, IL-1beta and IL-6. Chronobiol Int, 36(1), 11–26.Google Scholar
Roenneberg, T., Pilz, L. K., Zerbini, G., & Winnebeck, E. C. (2019). Chronotype and social jetlag: A (self-) critical review. Biology, 8(3), 54.Google Scholar
Said, E. A., Al-Abri, M. A., Al-Saidi, I., Al-Balushi, M. S., Al-Busaidi, J. Z., Al-Reesi, I., Koh, C. Y., Idris, M. A., Al-Jabri, A. A., & Habbal, O. (2019). Sleep deprivation alters neutrophil functions and levels of Th1-related chemokines and CD4(+) T cells in the blood. Sleep Breath, 23(4), 1331–1339.Google Scholar
Scheiermann, C., Gibbs, J. E., Ince, L., & Loudon, A. S. I. (2018). Clocking in to immunity. Nature Rev Immunol, 18, 423–437.Google Scholar
Silver, A. C., Arjona, A., Walker, W. E., & Fikrig, E. (2012). The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity, 36(2), 251–261.CrossRefGoogle ScholarPubMed
Sookoian, S., Gemma, C., Fernandez Gianotti, T., Burgueno, A., Alvarez, A., Gonzalez, C. D., & Pirola, C. J. (2007). Effects of rotating shift work on biomarkers of metabolic syndrome and inflammation. J Intern Med, 261(3), 285–292.Google Scholar
Souza, R. V., Sarmento, R. A., de Almeida, J. C., & Canuto, R. (2019). The effect of shift work on eating habits: a systematic review. Scand J Work Environ Health, 45(1), 7–21.Google Scholar
Spengler, M. L., Kuropatwinski, K. K., Comas, M., Gasparian, A. V., Fedtsova, N., Gleiberman, A. S., Gitlin, I. I., Artemicheva, N. M., Deluca, K. A., Gudkov, A. V., & Antoch, M. P. (2012). Core circadian protein CLOCK is a positive regulator of NF-κB-mediated transcription. Proc Natl Acad Sci USA, 109(37), E2457–E2465.Google Scholar
Timmons, G. A., O’Siorain, J. R., Kennedy, O. D., Curtis, A. M., & Early, J. O. (2020). Innate rhythms: Clocks at the center of monocyte and macrophage function. Front Immunol, 11, 1743.Google Scholar
Toh, K. L., Jones, C. R., He, Y., Eide, E. J., Hinz, W. A., Virshup, D. M., Ptacek, L. J., & Fu, Y. H. (2001). An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science, 291(5506), 1040–1043.Google Scholar
U.S. Bureau of Labor Statistics. (2019). Job Flexibilities and Work Schedules Summary. (USDL-19-1691). Available at: www.bls.gov/news.release/flex2.nr0.htm.Google Scholar
Vendelin, J., Bruce, S., Holopainen, P., Pulkkinen, V., Rytilä, P., Pirskanen, A., Rehn, M., Laitinen, T., Laitinen, L. A., Haahtela, T., Saarialho-Kere, U., Laitinen, A., & Kere, J. (2006). Downstream target genes of the neuropeptide S–NPSR1 pathway. Hum Mol Genet, 15(19), 2923–2935.Google Scholar
Walker, W. H., 2nd, Bumgarner, J. R., Becker-Krail, D. D., May, L. E., Liu, J. A., & Nelson, R. J. (2022). Light at night disrupts biological clocks, calendars, and immune function. Semin Immunopathol, 44(2), 165–173.Google Scholar
Wang, C., Lutes, L. K., Barnoud, C., & Scheiermann, C. (2022). The circadian immune system. Sci Immunol, 7(72), eabm2465.Google Scholar
Wang, S., Lin, Y., Li, F., Qin, Z., Zhou, Z., Gao, L., Yang, Z., Wang, Z., & Wu, B. (2020). An NF-kappaB-driven lncRNA orchestrates colitis and circadian clock. Sci Adv, 6(42), eabb5202.Google Scholar
Wang, S., Lin, Y., Yuan, X., Li, F., Guo, L., & Wu, B. (2018). REV-ERBalpha integrates colon clock with experimental colitis through regulation of NF-kappaB/NLRP3 axis. Nat Commun, 9(1), 4246.Google Scholar
Wehrens, S. M. T., Christou, S., Isherwood, C., Middleton, B., Gibbs, M. A., Archer, S. N., Skene, D. J., & Johnston, J. D. (2017). Meal timing regulates the human circadian system. Curr Biol, 27(12), 1768–1775 e1763.Google Scholar
Weintraub, Y., Cohen, S., Chapnik, N., Ben-Tov, A., Yerushalmy-Feler, A., Dotan, I., Tauman, R., & Froy, O. (2020). Clock gene disruption is an initial manifestation of inflammatory bowel diseases. Clin Gastroenterol Hepatol, 18(1), 115–122 e111.Google Scholar
Wittmann, M., Dinich, J., Merrow, M., & Roenneberg, T. (2006). Social jetlag: Misalignment of biological and social time. Chronobiol Int, 23(1–2), 497–509.Google Scholar
Wright, K. P. Jr., Drake, A. L., Frey, D. J., Fleshner, M., Desouza, C. A., Gronfier, C., & Czeisler, C. A. (2015). Influence of sleep deprivation and circadian misalignment on cortisol, inflammatory markers, and cytokine balance. Brain Behav Immun, 47, 24–34.Google Scholar
Xu, Y., Padiath, Q. S., Shapiro, R. E., Jones, C. R., Wu, S. C., Saigoh, N., Saigoh, K., Ptacek, L. J., & Fu, Y. H. (2005). Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature, 434(7033), 640–644.Google Scholar
Xu, Y., Toh, K. L., Jones, C. R., Shin, J. Y., Fu, Y. H., & Ptacek, L. J. (2007). Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell, 128(1), 59–70.Google Scholar
Yagita, K., Horie, K., Koinuma, S., Nakamura, W., Yamanaka, I., Urasaki, A., Shigeyoshi, Y., Kawakami, K., Shimada, S., Takeda, J., & Uchiyama, Y. (2010). Development of the circadian oscillator during differentiation of mouse embryonic stem cells in vitro. Proc Natl Acad Sci USA, 107(8), 3846–3851.Google Scholar
Yao, H., Sundar, I. K., Huang, Y., Gerloff, J., Sellix, M. T., Sime, P. J., & Rahman, I. (2015). Disruption of sirtuin 1-mediated control of circadian molecular clock and inflammation in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol, 53(6), 782–792.Google Scholar
Zhang, L., Hirano, A., Hsu, P.-K., Jones, C. R., Sakai, N., Okuro, M., McMahon, T., Yamazaki, M., Xu, Y., Saigoh, N., Saigoh, K., Lin, S.-T., Kaasik, K., Nishino, S., Ptáček, L. J., & Fu, Y.-H. (2016). A PERIOD3 variant causes a circadian phenotype and is associated with a seasonal mood trait. Proc Natl Acad Sci, 113(11), E1536–E1544.Google Scholar
Zimberg, I. Z., Fernandes Junior, S. A., Crispim, C. A., Tufik, S., & de Mello, M. T. (2012). Metabolic impact of shift work. Work, 41(Suppl 1), 4376–4383.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×