The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock

Brooks, John F.; Behrendt, Cassie L.; Ruhn, Kelly A.; Lee, Syann; Raj, Prithvi; Takahashi, Joseph S.; Hooper, Lora V.

doi:10.1016/j.cell.2021.07.001

Cited by 122 publications

(156 citation statements)

References 62 publications

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“…The circadian clock has recently been shown to play a role in the rhythms of the microbial response, and the Antimicrobial Peptide (AMP) gene expression of both Reg3g and Lcn2 exhibits diurnal rhythms ( Bellet et al., 2013 ; Brooks et al., 2021 ). We therefore tested the expression of AMPs in untreated mice and mice treated with DSS to induce colitis (all samples collected at ZT16, when Reg3g and Lcn2 have been shown to be higher).…”

Section: Resultsmentioning

confidence: 99%

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BMAL1 Regulates the Daily Timing of Colitis

Taleb

Carmona‐Alcocer

Stokes

et al. 2022

Front. Cell. Infect. Microbiol.

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Many physiological functions exhibit circadian rhythms: oscillations in biological processes that occur in a 24-hour period. These daily rhythms are maintained through a highly conserved molecular pacemaker known as the circadian clock. Circadian disruption has been proposed to cause increased risk of Inflammatory Bowel Disease (IBD) but the underlying mechanisms remain unclear. Patients with IBD experience chronic inflammation and impaired regeneration of intestinal epithelial cells. Previous animal-based studies have revealed that colitis models of IBD are more severe in mice without a circadian clock but the timing of colitis, and whether its inflammatory and regenerative processes have daily rhythms, remains poorly characterized. We tested circadian disruption using Bmal1-/- mutant mice that have a non-functional circadian clock and thus no circadian rhythms. Dextran Sulfate Sodium (DSS) was used to induce colitis. The disease activity of colitis was found to exhibit time-dependent variation in Bmal1+/+ control mice but is constant and elevated in Bmal1-/- mutants, who exhibit poor recovery. Histological analyses indicate worsened colitis severity in Bmal1-/- mutant colon, and colon infiltration of immune system cells shows a daily rhythm that is lost in the Bmal1-/- mutant. Similarly, epithelial proliferation in the colon has a daily rhythm in Bmal1+/+ controls but not in Bmal1-/- mutants. Our results support a critical role of a functional circadian clock in the colon which drives 24-hour rhythms in inflammation and healing, and whose disruption impairs colitis recovery. This indicates that weakening circadian rhythms not only worsens colitis, but delays healing and should be taken into account in the management of IBD. Recognition of this is important in the management of IBD patients required to do shift work.

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Section: Resultsmentioning

confidence: 99%

“…The primers used are listed in Supplementary Table 2 . Primer sequences were obtained from PrimerBank, Brooks et al (2021) , Kwon et al (2019) and Yamazaki et al (2011) . All gene expression was normalized to Gapdh .…”

Section: Methodsmentioning

confidence: 99%

BMAL1 Regulates the Daily Timing of Colitis

Taleb

Carmona‐Alcocer

Stokes

et al. 2022

Front. Cell. Infect. Microbiol.

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“…Although SARS-CoV-2 primarily infects the upper and lower respiratory tract, several lines of evidence have demonstrated viral replication within intestinal epithelial cells in the gut [ 38 , 42 , 43 ]. Given the role of the gut microbiota in regulating immune function and the biological clock at both systemic and local levels [ 44 – 46 ], and that SARS-CoV-2 infection can perturb the gut microbiota [ 47 ], it is plausible that improving gut microbiota diversity by personalised nutrition and supplementation could be beneficial to reduce disease severity, especially in elderly and immune-compromised patients.…”

Section: Respiratory Infectionsmentioning

confidence: 99%

The role of circadian clock pathways in viral replication

2022

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The daily oscillations of bi ological and behavioural processes are controlled by the circadian clock circuitry that drives the physiology of the organism and, in particular, the functioning of the immune system in response to infectious agents. Circadian rhythmicity is known to affect both the pharmacokinetics and pharmacodynamics of pharmacological agents and vaccine-elicited immune responses. A better understanding of the role circadian pathways play in the regulation of virus replication will impact our clinical management of these diseases. This review summarises the experimental and clinical evidence on the interplay between different viral pathogens and our biological clocks, emphasising the importance of continuing research on the role played by the biological clock in virus-host organism interaction.

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“…Furthermore, the symbiosis between the host and gut microbiota plays a critical role in maintaining the homeostasis of the host and dysbiosis of microbiota, which accounts for immune dysregulation and an impaired digestive system and metabolism (Knight and Girling, 2003;Thaiss et al, 2014). Symbiotic microbiota functions to bridge circadian rhythms with diverse effects, including development immunity and metabolism (Brooks et al, 2021;Kuang et al, 2019;Thaiss et al, 2014;Ma et al, 2019;Collado et al, 2018). Much evidence has revealed that space environment factors or analog conditions (e.g., microgravity, radiation, low fluid shear, and diet) cause altered composition of gut microbiota (Siddiqui et al, 2021;Acres et al, 2021;Cervantes and Hong, 2016;Saei and Barzegari et al, 2012;Li et al, 2015;Jiang et al, 2019).…”

Section: Social and Interspecies Interactionmentioning

confidence: 99%

How to Live on Mars With a Proper Circadian Clock?

Luo

Huang

et al. 2022

Front. Astron. Space Sci.

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Intrinsic circadian clocks generate circadian rhythms of physiology and behavior, which provide the capabilities to adapt to cycling environmental cues that result from the self-rotation of the Earth. Circadian misalignment leads to deleterious impacts on adaptation and health in different organisms. The environmental cues on the interplanetary journey to and on Mars dramatically differ from those on Earth. These differences impose numerous adaptive challenges, including challenges for humans’ circadian clock. Thus, adaptation of circadian rhythms to the Martian environment is a prerequisite for future landing and dwelling on Mars. Here, we review the progress of studies associated with the influence of the Martian environment on circadian rhythms and propose directions for further study and potential strategies to improve the adaptation of the circadian clock for future Mars missions.

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The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock

Cited by 122 publications

References 62 publications

BMAL1 Regulates the Daily Timing of Colitis

BMAL1 Regulates the Daily Timing of Colitis

The role of circadian clock pathways in viral replication

How to Live on Mars With a Proper Circadian Clock?

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