Top

Published in:

01-03-2022 | Vaccination | Review

Circadian rhythms in adaptive immunity and vaccination

Authors: Nicolas Cermakian, Sophia K. Stegeman, Kimaya Tekade, Nathalie Labrecque

Published in: Seminars in Immunopathology | Issue 2/2022

Abstract

Adaptive immunity allows an organism to respond in a specific manner to pathogens and other non-self-agents. Also, cells of the adaptive immune system, such as T and B lymphocytes, can mediate a memory of an encounter with a pathogen, allowing a more efficient response to a future infection. As for other aspects of physiology and of the immune system, the adaptive immune system is regulated by circadian clocks. Consequently, the development, differentiation, and trafficking between tissues of adaptive immune cells have been shown to display daily rhythms. Also, the response of T cells to stimuli (e.g., antigen presentation to T cells by dendritic cells) varies according to a circadian rhythm, due to T cell-intrinsic mechanisms as well as cues from other tissues. The circadian control of adaptive immune response has implications for our understanding of the fight against pathogens as well as auto-immune diseases, but also for vaccination, a preventive measure based on the development of immune memory.

Nobis CC, Labrecque N, Cermakian N (2018) From immune homeostasis to inflammation, a question of rhythms. Curr Opin Physio 5:90–98CrossRef

Duguay D, Cermakian N (2009) The crosstalk between physiology and circadian clock proteins. Chronobiol Int 26:1479–1513. https://doi.org/10.3109/07420520903497575CrossRefPubMed

Fortier EE, Rooney J, Dardente H, Hardy MP, Labrecque N, Cermakian N (2011) Circadian variation of the response of T cells to antigen. J Immunol 187:6291–6300. https://doi.org/10.4049/jimmunol.1004030CrossRefPubMed

Keller M, Mazuch J, Abraham U et al (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci U S A 106:21407–21412CrossRef

Silver AC, Arjona A, Hughes ME, Nitabach MN, Fikrig E (2012) Circadian expression of clock genes in mouse macrophages, dendritic cells, and B cells. Brain Behav Immun 26:407–413. https://doi.org/10.1016/j.bbi.2011.10.001CrossRefPubMed

Druzd D, Matveeva O, Ince L et al (2017) Lymphocyte circadian clocks control lymph node trafficking and adaptive immune responses. Immunity 46:120–132. https://doi.org/10.1016/j.immuni.2016.12.011CrossRefPubMedPubMedCentral

Hemmers S, Rudensky AY (2015) The cell-intrinsic circadian clock is dispensable for lymphocyte differentiation and function. Cell Rep 11:1339–1349. https://doi.org/10.1016/j.celrep.2015.04.058CrossRefPubMedPubMedCentral

Hand LE, Gray KJ, Dickson SH et al (2020) Regulatory T cells confer a circadian signature on inflammatory arthritis. Nat Commun 11:1658. https://doi.org/10.1038/s41467-020-15525-0CrossRefPubMedPubMedCentral

Hopwood TW, Hall S, Begley N et al (2018) The circadian regulator BMAL1 programmes responses to parasitic worm infection via a dendritic cell clock. Sci Rep 8:3782. https://doi.org/10.1038/s41598-018-22021-5CrossRefPubMedPubMedCentral

10.

Nobis CC, Dubeau Laramee G, Kervezee L, Maurice De Sousa D, 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 U S A 116:20077–20086. https://doi.org/10.1073/pnas.1905080116CrossRefPubMedPubMedCentral

11.

Bollinger T, Leutz A, Leliavski A et al (2011) Circadian clocks in mouse and human CD4+ T cells. PLoS ONE 6:e29801. https://doi.org/10.1371/journal.pone.0029801CrossRefPubMedPubMedCentral

12.

Cuesta M, Boudreau P, Cermakian N, Boivin DB (2017) Rapid resetting of human peripheral clocks by phototherapy during simulated night shift work. Sci Rep 7:16310. https://doi.org/10.1038/s41598-017-16429-8CrossRefPubMedPubMedCentral

13.

Boivin DB, James FO, Wu A, Cho-Park PF, Xiong H, Sun ZS (2003) Circadian clock genes oscillate in human peripheral blood mononuclear cells. Blood 102:4143–4145CrossRef

14.

Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB (2014) A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci U S A 111:16219–16224. https://doi.org/10.1073/pnas.1408886111CrossRefPubMedPubMedCentral

15.

Collins EJ, Cervantes-Silva MP, Timmons GA, O’Siorain JR, Curtis AM, Hurley JM (2021) Post-transcriptional circadian regulation in macrophages organizes temporally distinct immunometabolic states. Genome Res. https://doi.org/10.1101/gr.263814.120CrossRefPubMedPubMedCentral

16.

Depres-Brummer P, Bourin P, Pages N, Metzger G, Levi F (1997) Persistent T lymphocyte rhythms despite suppressed circadian clock outputs in rats. Am J Physiol 273:R1891-1899PubMed

17.

Kawate T, Abo T, Hinuma S, Kumagai K (1981) Studies of the bioperiodicity of the immune response. II. Co-variations of murine T and B cells and a role of corticosteroid. J Immunol 126:1364–1367PubMed

18.

Abo T, Kawate T, Itoh K, Kumagai K (1981) Studies on the bioperiodicity of the immune response. I. Circadian rhythms of human T, B, and K cell traffic in the peripheral blood. J Immunol 126:1360–1363PubMed

19.

Born J, Lange T, Hansen K, Molle M, Fehm HL (1997) Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol 158:4454–4464PubMed

20.

Cuesta M, Boudreau P, Dubeau-Laramee G, Cermakian N, Boivin DB (2016) Simulated night shift disrupts circadian rhythms of immune functions in humans. J Immunol 196:2466–2475. https://doi.org/10.4049/jimmunol.1502422CrossRefPubMed

21.

Dimitrov S, Benedict C, Heutling D, Westermann J, Born J, Lange T (2009) Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. Blood 113:5134–5143CrossRef

22.

Kirsch S, Thijssen S, Alarcon Salvador S et al (2012) T-cell numbers and antigen-specific T-cell function follow different circadian rhythms. J Clin Immunol 32:1381–1389. https://doi.org/10.1007/s10875-012-9730-zCrossRefPubMed

23.

Miyawaki T, Taga K, Nagaoki T, Seki H, Suzuki Y, Taniguchi N (1984) Circadian changes of T lymphocyte subsets in human peripheral blood. Clin Exp Immunol 55:618–622PubMedPubMedCentral

24.

Dimitrov S, Lange T, Nohroudi K, Born J (2007) Number and function of circulating human antigen presenting cells regulated by sleep. Sleep 30:401–411. https://doi.org/10.1093/sleep/30.4.401CrossRefPubMed

25.

Dijk DJ, Duffy JF, Czeisler CA (1992) Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1:112–117. https://doi.org/10.1111/j.1365-2869.1992.tb00021.xCrossRefPubMed

26.

Besedovsky L, Born J, Lange T (2014) Endogenous glucocorticoid receptor signaling drives rhythmic changes in human T-cell subset numbers and the expression of the chemokine receptor CXCR4. FASEB J 28:67–75. https://doi.org/10.1096/fj.13-237958CrossRefPubMed

27.

Shimba A, Cui G, Tani-Ichi S et al (2018) Glucocorticoids drive diurnal oscillations in T cell distribution and responses by inducing interleUkin-7 receptor and CXCR4. Immunity 48(286–298):e286. https://doi.org/10.1016/j.immuni.2018.01.004CrossRef

28.

Suzuki K, Hayano Y, Nakai A, Furuta F, Noda M (2016) Adrenergic control of the adaptive immune response by diurnal lymphocyte recirculation through lymph nodes. J Exp Med 213:2567–2574. https://doi.org/10.1084/jem.20160723CrossRefPubMedPubMedCentral

29.

Suzuki S, Toyabe S, Moroda T et al (1997) Circadian rhythm of leucocytes and lymphocytes subsets and its possible correlation with the function of the autonomic nervous system. Clin Exp Immunol 110:500–508. https://doi.org/10.1046/j.1365-2249.1997.4411460.xCrossRefPubMedPubMedCentral

30.

Sengupta S, Tang SY, Devine JC et al (2019) Circadian control of lung inflammation in influenza infection. Nat Commun 10:4107. https://doi.org/10.1038/s41467-019-11400-9CrossRefPubMedPubMedCentral

31.

Tavadia HB, Fleming KA, Hume PD, Simpson HW (1975) Circadian rhythmicity of human plasma cortisol and PHA-induced lymphocyte transformation. Clin Exp Immunol 22:190–193PubMedPubMedCentral

32.

Esquifino AI, Alvarez MP, Cano P, Chacon F, Reyes Toso CF, Cardinali DP (2004) 24-hour pattern of circulating prolactin and growth hormone levels and submaxillary lymph node immune responses in growing male rats subjected to social isolation. Endocrine 25:41–48CrossRef

33.

Esquifino AI, Selgas L, Arce A, Maggiore VD, Cardinali DP (1996) Twenty-four-hour rhythms in immune responses in rat submaxillary lymph nodes and spleen: effect of cyclosporine. Brain Behav Immun 10:92–102CrossRef

34.

Kaplan MS, Byers VS, Levin AS, German DF, Fudenberg HH, Lecam LN (1976) Circadian rhythm of stimulated lymphocyte blastogenesis. A 24 hour cycle in the mixed leukocyte culture reaction and with SKSD stimulation. J Allergy Clin Immunol 58:180–189. https://doi.org/10.1016/0091-6749(76)90153-6CrossRefPubMed

35.

Hiemke C, Brunner R, Hammes E, Muller H, Meyerz um Buschenfelde KH, Lohse AW (1995) Circadian variations in antigen-specific proliferation of human T lymphocytes and correlation to cortisol production. Psychoneuroendocrinology 20:335–342CrossRef

36.

Silver AC, Arjona A, Walker WE, Fikrig E (2012) The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36:251–261. https://doi.org/10.1016/j.immuni.2011.12.017CrossRefPubMedPubMedCentral

37.

Nguyen KD, Fentress SJ, Qiu Y, Yun K, Cox JS, Chawla A (2013) Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 341:1483–1488. https://doi.org/10.1126/science.1240636CrossRefPubMed

38.

Amir M, Campbell S, Kamenecka TM, Solt LA (2020) Pharmacological modulation and genetic deletion of REV-ERBalpha and REV-ERBbeta regulates dendritic cell development. Biochem Biophys Res Commun 527:1000–1007. https://doi.org/10.1016/j.bbrc.2020.05.012CrossRefPubMedPubMedCentral

39.

Holtkamp SJ, Ince LM, Barnoud C et al (2021) Circadian clocks guide dendritic cells into skin lymphatics. Nat Immunol. https://doi.org/10.1038/s41590-021-01040-xCrossRefPubMedPubMedCentral

40.

Tuganbaev T, Mor U, Bashiardes S et al (2020) Diet diurnally regulates small intestinal microbiome-epithelial-immune homeostasis and enteritis. Cell 182(1441–1459):e1421. https://doi.org/10.1016/j.cell.2020.08.027CrossRef

41.

Sutton CE, Finlay CM, Raverdeau M et al (2017) Loss of the molecular clock in myeloid cells exacerbates T cell-mediated CNS autoimmune disease. Nat Commun 8:1923CrossRef

42.

Yu X, Rollins D, Ruhn KA et al (2013) TH17 cell differentiation is regulated by the circadian clock. Science 342:727–730. https://doi.org/10.1126/science.1243884CrossRefPubMedPubMedCentral

43.

Male V, Nisoli I, Gascoyne DM, Brady HJ (2012) E4BP4: an unexpected player in the immune response. Trends Immunol 33:98–102. https://doi.org/10.1016/j.it.2011.10.002CrossRefPubMed

44.

Amir M, Chaudhari S, Wang R et al (2018) REV-ERBalpha regulates TH17 cell development and autoimmunity. Cell Rep 25(3733–3749):e3738. https://doi.org/10.1016/j.celrep.2018.11.101CrossRef

45.

Chang C, Loo CS, Zhao X et al (2019) The nuclear receptor REV-ERBalpha modulates Th17 cell-mediated autoimmune disease. Proc Natl Acad Sci U S A 116:18528–18536. https://doi.org/10.1073/pnas.1907563116CrossRefPubMedPubMedCentral

46.

Farez MF, Mascanfroni ID, Mendez-Huergo SP et al (2015) Melatonin contributes to the seasonality of multiple sclerosis relapses. Cell 162:1338–1352. https://doi.org/10.1016/j.cell.2015.08.025CrossRefPubMedPubMedCentral

47.

Kennaway DJ (2019) Melatonin research in mice: a review. Chronobiol Int 36:1167–1183. https://doi.org/10.1080/07420528.2019.1624373CrossRefPubMed

48.

Hand LE, Hopwood TW, Dickson SH et al (2016) The circadian clock regulates inflammatory arthritis. FASEB J 30:3759–3770. https://doi.org/10.1096/fj.201600353RCrossRefPubMedPubMedCentral

49.

Hand LE, Dickson SH, Freemont AJ, Ray DW, Gibbs JE (2019) The circadian regulator Bmal1 in joint mesenchymal cells regulates both joint development and inflammatory arthritis. Arthritis Res Ther 21:5. https://doi.org/10.1186/s13075-018-1770-1CrossRefPubMedPubMedCentral

50.

Sun Y, Yang Z, Niu Z et al (2006) MOP3, a component of the molecular clock, regulates the development of B cells. Immunology

51.

Fernandes G, Halberg F, Yunis EJ, Good RA (1976) Circadian rhythmic plaque-forming cell response of spleens from mice immunized with SRBC. J Immunol 117:962–966PubMed

52.

Cao Q, Zhao X, Bai J et al (2017) Circadian clock cryptochrome proteins regulate autoimmunity. Proc Natl Acad Sci U S A 114:12548–12553. https://doi.org/10.1073/pnas.1619119114CrossRefPubMedPubMedCentral

53.

Prentice S, Dockrell HM (2020) Antituberculosis BCG vaccination: more reasons for varying innate and adaptive immune responses. J Clin Invest 130:5121–5123. https://doi.org/10.1172/JCI141317CrossRefPubMedPubMedCentral

54.

Langlois PH, Smolensky MH, Glezen WP, Keitel WA (1995) Diurnal variation in responses to influenza vaccine. Chronobiol Int 12:28–36. https://doi.org/10.3109/07420529509064497CrossRefPubMed

55.

Long JE, Drayson MT, Taylor AE, Toellner KM, Lord JM, Phillips AC (2016) Morning vaccination enhances antibody response over afternoon vaccination: a cluster-randomised trial. Vaccine 34:2679–2685. https://doi.org/10.1016/j.vaccine.2016.04.032CrossRefPubMedPubMedCentral

56.

Phillips AC, Gallagher S, Carroll D, Drayson M (2008) Preliminary evidence that morning vaccination is associated with an enhanced antibody response in men. Psychophysiology 45:663–666. https://doi.org/10.1111/j.1469-8986.2008.00662.xCrossRefPubMed

57.

Karabay O, Temel A, Koker AG, Tokel M, Ceyhan M, Kocoglu E (2008) Influence of circadian rhythm on the efficacy of the hepatitis B vaccination. Vaccine 26:1143–1144. https://doi.org/10.1016/j.vaccine.2007.12.046CrossRefPubMed

58.

Gottlob S, Gille C, Poets CF (2019) Randomized controlled trial on the effects of morning versus evening primary vaccination on episodes of hypoxemia and bradycardia in very preterm infants. Neonatology 116:315–320. https://doi.org/10.1159/000501338CrossRefPubMed

59.

de Bree LCJ, Mourits VP, Koeken VA et al (2020) Circadian rhythm influences induction of trained immunity by BCG vaccination. J Clin Invest 130:5603–5617. https://doi.org/10.1172/JCI133934CrossRefPubMedPubMedCentral

60.

Lange T, Dimitrov S, Born J (2010) Effects of sleep and circadian rhythm on the human immune system. Ann N Y Acad Sci 1193:48–59. https://doi.org/10.1111/j.1749-6632.2009.05300.xCrossRefPubMed

61.

Benedict C, Cedernaes J (2021) Could a good night’s sleep improve COVID-19 vaccine efficacy? Lancet Respir Med 9:447–448. https://doi.org/10.1016/S2213-2600(21)00126-0CrossRefPubMedPubMedCentral

62.

Lange T, Dimitrov S, Bollinger T, Diekelmann S, Born J (2011) Sleep after vaccination boosts immunological memory. J Immunol 187:283–290. https://doi.org/10.4049/jimmunol.1100015CrossRefPubMed

63.

Lange T, Perras B, Fehm HL, Born J (2003) Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom Med 65:831–835. https://doi.org/10.1097/01.psy.0000091382.61178.f1CrossRefPubMed

64.

Benedict C, Brytting M, Markstrom A, Broman JE, Schioth HB (2012) Acute sleep deprivation has no lasting effects on the human antibody titer response following a novel influenza A H1N1 virus vaccination. BMC Immunol 13:1. https://doi.org/10.1186/1471-2172-13-1CrossRefPubMedPubMedCentral

65.

Prather AA, Hall M, Fury JM, Ross DC, Muldoon MF, Cohen S, Marsland AL (2012) Sleep and antibody response to hepatitis B vaccination. Sleep 35:1063–1069. https://doi.org/10.5665/sleep.1990CrossRefPubMedPubMedCentral

66.

Bjorvatn B, Axelsson J, Pallesen S et al (2020) The association between shift work and immunological biomarkers in nurses. Front Public Health 8:415. https://doi.org/10.3389/fpubh.2020.00415CrossRefPubMedPubMedCentral

67.

Ruiz FS, Rosa DS, Zimberg IZ et al (2020) Night shift work and immune response to the meningococcal conjugate vaccine in healthy workers: a proof of concept study. Sleep Med 75:263–275. https://doi.org/10.1016/j.sleep.2020.05.032CrossRefPubMed

68.

Kervezee L, Kosmadopoulos A, Boivin DB (2020) Metabolic and cardiovascular consequences of shift work: the role of circadian disruption and sleep disturbances. Eur J Neurosci 51:396–412. https://doi.org/10.1111/ejn.14216CrossRefPubMed

Title: Circadian rhythms in adaptive immunity and vaccination
Authors: Nicolas Cermakian
Sophia K. Stegeman
Kimaya Tekade
Nathalie Labrecque
Publication date: 01-03-2022
Publisher: Springer Berlin Heidelberg
Keyword: Vaccination
Published in: Seminars in Immunopathology / Issue 2/2022
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-021-00903-7

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2022

Chronoimmunology: from preclinical assessments to clinical applications

Glucocorticoid circadian rhythms in immune function

Light at night disrupts biological clocks, calendars, and immune function

Adaptive immunity, chronic inflammation and the clock

Circadian regulation of innate immunity in animals and humans and implications for human disease

Intertwining roles of circadian and metabolic regulation of the innate immune response

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials