474
Views
2
CrossRef citations to date
0
Altmetric
Review

The circadian rhythm of viruses and its implications on susceptibility to infection

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 1109-1117 | Received 11 Feb 2022, Accepted 27 Apr 2022, Published online: 11 May 2022

References

  • Callaway E, Ledford H. Medicine Nobel awarded for work on circadian clocks. Nature. 2017;550(7674):18.
  • Burki T. Nobel prize awarded for discoveries in circadian rhythm. Lancet. 2017;390(10104):e25.
  • Scheiermann C, Kunisaki Y, Frenette PS. Circadian control of the immune system. Nat Rev Immunol. 2013;13(3):190–198.
  • Yousef E, Mitwally N, Noufal N, et al. Shift work and risk of skin cancer: a systematic review and meta-analysis. Sci Rep. 2020;10(1):2012.
  • He C, Anand ST, Ebell MH, et al. Circadian disrupting exposures and breast cancer risk: a meta-analysis. Int Arch Occup Environ Health. 2015;88(5):533–547.
  • Edgar RS, Stangherlin A, Nagy AD, et al. Cell autonomous regulation of herpes and influenza virus infection by the circadian clock. Proc Natl Acad Sci U S A. 2016;113(36):10085–10090.
  • Reddy AB, O’Neill JS. Healthy clocks, healthy body, healthy mind. Trends Cell Biol. 2010;20(1):36–44.
  • Staels B. When the clock stops ticking, metabolic syndrome explodes. Nat Med. 2006;12(1):54–55. discussion 55.
  • Liu Z, Yu K, Zheng J, et al. Dysregulation, functional implications, and prognostic ability of the circadian clock across cancers. Cancer Med. 2019;8(4):1710–1720.
  • Borrmann H, McKeating JA, Zhuang X. The circadian clock and viral infections. J Biol Rhythms. 2021;36(1):9–22.
  • Rijo-Ferreira F, Takahashi JS. Circadian rhythms in infectious diseases and symbiosis. Semin Cell Dev Biol. 2021. DOI:https://doi.org/10.1016/j.semcdb.2021.09.004
  • Tognini P, Murakami M, Sassone-Corsi P. Interplay between microbes and the circadian clock. Cold Spring Harb Perspect Biol. 2018;10(9):a028365.
  • Zhuang X, Rambhatla SB, Lai AG, et al. Interplay between circadian clock and viral infection. J Mol Med (Berl). 2017;95(12):1283–1289.
  • Diallo AB, Coiffard B, Leone M, et al. For whom the clock ticks: clinical chronobiology for infectious diseases. Front Immunol. 2020;11:1457.
  • Murakami M, Tognini P. The circadian clock as an essential molecular link between host physiology and microorganisms. Front Cell Infect Microbiol. 2019;9:469.
  • Barik S. Molecular interactions between pathogens and the circadian clock. Int J Mol Sci. 2019;20(23):5824.
  • Pearson JA, Voisey AC, Boest-Bjerg K, et al. Circadian rhythm modulation of microbes during health and infection. Front Microbiol. 2021;12:721004.
  • Mazzoccoli G, Vinciguerra M, Carbone A, et al. The circadian clock, the immune system, and viral infections: the intricate relationship between biological time and host-virus interaction. Pathogens. 2020;9(2):83.
  • Abrahamson EE, Moore RY. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001;916(1–2):172–191.
  • Allada R, Bass J, Longo DL. Circadian mechanisms in medicine. N Engl J Med. 2021;384(6):550–561.
  • Scheiermann C, Gibbs J, Ince L, et al. Clocking in to immunity. Nat Rev Immunol. 2018;18(7):423–437.
  • Voigt RM, Summa KC, Forsyth CB, et al. The circadian clock mutation promotes intestinal dysbiosis. Alcohol Clin Exp Res. 2016;40(2):335–347.
  • Ko CH, Takahashi JS. Molecular components of the mammalian circadian clock. Hum Mol Genet. 2006;15(suppl_2):R271–277. 15 Spec No 2.
  • Gekakis N, Staknis D, Nguyen HB, et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science. 1998;280(5369):1564–1569.
  • Yoo SH, Ko CH, Lowrey PL, et al. A noncanonical E-box enhancer drives mouse period2 circadian oscillations in vivo. Proc Natl Acad Sci U S A. 2005;102(7):2608–2613.
  • Xu H, Gustafson CL, Sammons PJ, et al. Cryptochrome 1 regulates the circadian clock through dynamic interactions with the BMAL1 C terminus. Nat Struct Mol Biol. 2015;22(6):476–484.
  • Sengupta S, Ince L, Sartor F, et al. Clocks, viruses, and immunity: lessons for the COVID-19 pandemic. J Biol Rhythms. 2021;36(1):23–34.
  • Ehlers A, Xie W, Agapov E, et al. BMAL1 links the circadian clock to viral airway pathology and asthma phenotypes. Mucosal Immunol. 2018;11(1):97–111.
  • Majumdar T, Dhar J, Patel S, et al. Circadian transcription factor BMAL1 regulates innate immunity against select RNA viruses. Innate Immun. 2017;23(2):147–154.
  • Anderson G, Reiter RJ. Melatonin: roles in influenza, covid-19, and other viral infections. Rev Med Virol. 2020;30(3):e2109.
  • Sengupta S, Tang SY, Devine JC, et al. Circadian control of lung inflammation in influenza infection. Nat Commun. 2019;10(1):4107.
  • Costantini C, Renga G, Sellitto F, et al. Microbes in the era of circadian medicine. Front Cell Infect Microbiol. 2020;10:30.
  • Keller M, Mazuch J, Abraham U, et al. A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci U S A. 2009;106(50):21407–21412.
  • Ella K, Csepanyi-Komi R, Kaldi K. Circadian regulation of human peripheral neutrophils. Brain Behav Immun. 2016;57:209–221.
  • Pick R, He W, Chen CS, et al. Time-of-day-dependent trafficking and function of leukocyte subsets. Trends Immunol. 2019;40(6):524–537.
  • Nathan P, Gibbs JE, Rainger GE, et al. Changes in circadian rhythms dysregulate inflammation in ageing: focus on leukocyte trafficking. Front Immunol. 2021;12:673405.
  • Sundar IK, Ahmad T, Yao H, et al. Influenza A virus-dependent remodeling of pulmonary clock function in a mouse model of COPD. Sci Rep. 2015;4(1):9927.
  • Nguyen KD, Fentress SJ, Qiu Y, et al. Circadian gene bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science. 2013;341(6153):1483–1488.
  • Dowell SF. Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerg Infect Dis. 2001;7(3):369–374.
  • Dopico XC, Evangelou M, Ferreira RC, et al. Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nat Commun. 2015;6(1):7000.
  • Martinez ME, Kline KA. The calendar of epidemics: seasonal cycles of infectious diseases. PLoS Pathog. 2018;14(11):e1007327.
  • Matsuzawa T, Nakamura Y, Ogawa Y, et al. Differential day-night outcome to HSV-2 cutaneous infection. J Invest Dermatol. 2018;138(1):233–236.
  • Oliva-Ramirez J, Moreno-Altamirano MM, Pineda-Olvera B, et al. Crosstalk between circadian rhythmicity, mitochondrial dynamics and macrophage bactericidal activity. Immunology. 2014;143(3):490–497.
  • Gibbs JE, Blaikley J, Beesley S, et al. The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci U S A. 2012;109(2):582–587.
  • Timmons GA, O’Siorain JR, Kennedy OD, et al. Innate rhythms: clocks at the center of monocyte and macrophage function. Front Immunol. 2020;11:1743.
  • Benegiamo G, Mazzoccoli G, Cappello F, et al. Mutual antagonism between circadian protein period 2 and hepatitis C virus replication in hepatocytes. PLoS One. 2013;8(4):e60527.
  • Butler TD, Gibbs JE. Circadian host-microbiome interactions in immunity. Front Immunol. 2020;11:1783.
  • Brooks JF 2nd, Behrendt CL, Ruhn KA, et al. The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock. Cell. 2021;184(16):4154–4167 e4112.
  • Li N, Ma WT, Pang M, et al. The commensal microbiota and viral infection: a comprehensive review. Front Immunol. 2019;10:1551.
  • Yuan L, Hensley C, Mahsoub HM, et al. Microbiota in viral infection and disease in humans and farm animals. Prog Mol Biol Transl Sci. 2020;171:15–60.
  • Rafferty H, Murray MJ, Tam JCH, et al. Are the patterns of cytomegalovirus viral load seen after solid organ transplantation affected by circadian rhythm? J Infect Dis. 2022. DOI:https://doi.org/10.1093/infdis/jiac055.
  • Hepatitis B Available at: https://www.who.int/news-room/fact-sheets/detail/hepatitis-b.
  • Zhuang X, Forde D, Tsukuda S, et al. Circadian control of hepatitis B virus replication. Nat Commun. 2021;12(1):1658.
  • Qu M, Duffy T, Hirota T, et al. Nuclear receptor HNF4A transrepresses CLOCK:BMAL1 and modulates tissue-specific circadian networks. Proc Natl Acad Sci U S A. 2018;115(52):E12305–E12312.
  • Hepatitis C Available at: https://www.who.int/news-room/fact-sheets/detail/hepatitis-c.
  • Luna JM, Scheel TK, Danino T, et al. Hepatitis C virus RNA functionally sequesters miR-122. Cell. 2015;160(6):1099–1110.
  • Arjona A, Sarkar DK. Evidence supporting a circadian control of natural killer cell function. Brain Behav Immun. 2006;20(5):469–476.
  • Zhuang X, Lai AG, McKeating JA, et al. Daytime variation in hepatitis C virus replication kinetics following liver transplant. Wellcome Open Res. 2018;3(96):96.
  • Zhuang X, Magri A, Hill M, et al. The circadian clock components BMAL1 and REV-ERBα regulate flavivirus replication. Nat Commun. 2019;10(1):377.
  • HIV/AIDS. Available at: https://www.who.int/news-room/fact-sheets/detail/hiv-aids.
  • Zhao L, Liu M, Ouyang J, et al. The per-1 short isoform inhibits de novo HIV-1 transcription in resting CD4+ T-cells. Curr HIV Res. 2018;16(6):384–395.
  • Borrmann H, Davies R, Dickinson M, et al. Pharmacological activation of the circadian component REV-ERB inhibits HIV-1 replication. Sci Rep. 2020;10(1):13271.
  • Chang CC, Naranbhai V, Stern J, et al. Variation in cell-associated unspliced HIV RNA on antiretroviral therapy is associated with the circadian regulator brain-and-muscle-ARNT-like-1. AIDS. 2018;32(15):2119–2128.
  • Stern J, Solomon A, Dantanarayana A, et al. Cell-associated HIV RNA has a circadian cycle in males living with HIV on antiretroviral therapy. J Infect Dis. 2021. DOI:https://doi.org/10.1093/infdis/jiab533.
  • WHO Coronavirus. Available at: https://covid19.who.int.
  • Nosal C, Ehlers A, Haspel JA. Why lungs keep time: circadian rhythms and lung immunity. Annu Rev Physiol. 2020;82(1):391–412.
  • Gibbs J, Ince L, Matthews L, et al. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat Med. 2014;20(8):919–926.
  • Pariollaud M, Gibbs JE, Hopwood TW, et al. Circadian clock component REV-ERBalpha controls homeostatic regulation of pulmonary inflammation. J Clin Invest. 2018;128(6):2281–2296.
  • Herichova I, Zsoldosova K, Vesela A, et al. Effect of angiotensin II infusion on rhythmic clock gene expression and local renin-angiotensin system in the aorta of Wistar rats. Endocr Regul. 2014;48(3):144–151.
  • Zhuang X, Tsukuda S, Wrensch F, et al. The circadian clock component BMAL1 regulates SARS-CoV-2 entry and replication in lung epithelial cells. iScience. 2021;24(10):103144.
  • Diallo AB, Gay L, Coiffard B, et al. Daytime variation in SARS-CoV-2 infection and cytokine production. Microb Pathog. 2021;158:105067.
  • McNaughton CD, Adams NM, Hirschie Johnson C, et al. Diurnal variation in SARS-CoV-2 PCR test results: test accuracy may vary by time of day. J Biol Rhythms. 2021;36(6): 595–601.
  • Hunt T, Sassone-Corsi P. Riding tandem: circadian clocks and the cell cycle. Cell. 2007;129(3):461–464.
  • Fu L, Lee CC. The circadian clock: pacemaker and tumour suppressor. Nat Rev Cancer. 2003;3(5):350–361.
  • Ye Y, Xiang Y, Ozguc FM, et al. The genomic landscape and pharmacogenomic interactions of clock genes in cancer chronotherapy. Cell Syst. 2018;6(3):314–328 e312.
  • Fekry B, Eckel-Mahan K. The circadian clock and cancer: links between circadian disruption and disease pathology. J Biochem. 2022. DOI:https://doi.org/10.1093/jb/mvac017
  • Villanueva A, Longo DL. Hepatocellular carcinoma. N Engl J Med. 2019;380(15):1450–1462.
  • Cretenet G, Le Clech M, Gachon F. Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab. 2010;11(1):47–57.
  • Feng D, Liu T, Sun Z, et al. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science. 2011;331(6022):1315–1319.
  • Zhou L, Zhang Z, Nice E, et al. Circadian rhythms and cancers: the intrinsic links and therapeutic potentials. J Hematol Oncol. 2022;15(1):21.
  • Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol. 2007;47(1):593–628.
  • Baraldo M. The influence of circadian rhythms on the kinetics of drugs in humans. Expert Opin Drug Metab Toxicol. 2008;4(2):175–192.
  • Tsimakouridze EV, Alibhai FJ, Martino TA. Therapeutic applications of circadian rhythms for the cardiovascular system. Front Pharmacol. 2015;6:77.
  • Hermida RC, Ayala DE, Smolensky MH, et al. Chronotherapy improves blood pressure control and reduces vascular risk in CKD. Nat Rev Nephrol. 2013;9(6):358–368.
  • Lin Y, Wang S, Zhou Z, et al. Bmal1 regulates circadian expression of cytochrome P450 3a11 and drug metabolism in mice. Commun Biol. 2019;2(1):378.
  • Anzenbacher P, Anzenbacherova E. Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci. 2001;58(5–6):737–747.
  • Sanchez A, Calpena AC, Clares B. Evaluating the oxidative stress in inflammation: role of melatonin. Int J Mol Sci. 2015;16(8):16981–17004.
  • Pfeffer M, Korf HW, Wicht H. Synchronizing effects of melatonin on diurnal and circadian rhythms. Gen Comp Endocrinol. 2018;258:215–221.
  • Junaid A, Tang H, van Reeuwijk A, et al. Ebola hemorrhagic shock syndrome-on-a-Chip. iScience. 2020;23(1):100765.
  • Montiel M, Bonilla E, Valero N, et al. Melatonin decreases brain apoptosis, oxidative stress, and CD200 expression and increased survival rate in mice infected by Venezuelan equine encephalitis virus. Antivir Chem Chemother. 2015;24(3–4):99–108.
  • Morchang A, Malakar S, Poonudom K, et al. Melatonin inhibits dengue virus infection via the sirtuin 1-mediated interferon pathway. Viruses. 2021;13(4):659.
  • Zhou Y, Hou Y, Shen J, et al. A network medicine approach to investigation and population-based validation of disease manifestations and drug repurposing for COVID-19. PLoS Biol. 2020;18(11):e3000970.
  • Garcia-Garcia I, Seco-Meseguer E, Ruiz-Seco P, et al. Melatonin in the prophylaxis of SARS-CoV-2 infection in healthcare workers (MeCOVID): a randomised clinical trial. J Clin Med. 2022;11(4):1139.
  • Mousavi SA, Heydari K, Mehravaran H, et al. Melatonin effects on sleep quality and outcomes of COVID-19 patients: an open-label, randomized, controlled trial. J Med Virol. 2022;94(1):263–271.
  • Long JE, Drayson MT, Taylor AE, et al. Morning vaccination enhances antibody response over afternoon vaccination: a cluster-randomised trial. Vaccine. 2016;34(24):2679–2685.
  • Karabay O, Temel A, Koker AG, et al. Influence of circadian rhythm on the efficacy of the hepatitis B vaccination. Vaccine. 2008;26(9):1143–1144.
  • Hwang J, Jiang A, Fikrig E. Rev-erb agonist inhibits chikungunya and O’nyong’nyong virus replication. Open Forum Infect Dis. 2018;5(12):ofy315.
  • Gagnidze K, Hajdarovic KH, Moskalenko M, et al. Nuclear receptor REV-ERBalpha mediates circadian sensitivity to mortality in murine vesicular stomatitis virus-induced encephalitis. Proc Natl Acad Sci U S A. 2016;113(20):5730–5735.
  • Sultan A, Ali R, Sultan T, et al. Circadian clock modulating small molecules repurposing as inhibitors of SARS-CoV-2 M(pro) for pharmacological interventions in COVID-19 pandemic. Chronobiol Int. 2021;38(7):971–985.
  • Hirota T, Lee JW, St John PC, et al. Identification of small molecule activators of cryptochrome. Science. 2012;337(6098):1094–1097.
  • Ray S, Reddy AB. COVID-19 management in light of the circadian clock. Nat Rev Mol Cell Biol. 2020;21(9):494–495.
  • Vinciguerra M, Mazzoccoli G, Piccoli C, et al. Exploitation of host clock gene machinery by hepatitis viruses B and C. World J Gastroenterol. 2013;19(47):8902–8909.
  • Le Sage V, Cinti A, Amorim R, et al. Adapting the stress response: viral subversion of the mTOR signaling pathway. Viruses. 2016;8(6):152.
  • Lipton JO, Yuan ED, Boyle LM, et al. The circadian protein BMAL1 regulates translation in response to S6K1-mediated phosphorylation. Cell. 2015;161(5):1138–1151.
  • Wu R, Dang F, Li P, et al. The circadian protein period2 suppresses mTORC1 activity via recruiting Tsc1 to mTORC1 complex. Cell Metab. 2019;29(3):653–667 e656.
  • Zhuang X, Edgar RS, McKeating JA. The role of circadian clock pathways in viral replication. Semin Immunopathol. 2022;44(2):175–182.
  • Xiang K, Xu Z, Hu YQ, et al. Circadian clock genes as promising therapeutic targets for autoimmune diseases. Autoimmun Rev. 2021;20(8):102866.
  • Ferri C, Ursini F, Gragnani L, et al. Impaired immunogenicity to COVID-19 vaccines in autoimmune systemic diseases. high prevalence of non-response in different patients’ subgroups. J Autoimmun. 2021;125:102744.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.