Diurnal transcriptome landscape of a multi-tissue response to time-restricted feeding in mammals

Deota, Shaunak; Lin, Terry; Chaix, Amandine; Williams, April; Le, Hiep D.; Calligaro, Hugo; Ramasamy, Ramesh; Huang, Ling; Panda, Satchidananda

doi:10.1016/j.cmet.2022.12.006

Cited by 57 publications

(52 citation statements)

References 78 publications

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“…Several NRs displayed a robust 23 to 24-hours cycle ( Nr1d1 / Rev-erba, Nr1d2 / Rev-erbb, Nr1c2 / Pparb/d and Nr1f3 / Rorg ) while Nr2f6 / Ear2, Nr2b1 / Rxra, Nr1c1 / Ppara, Nr2c2 / Tr4, Nr1h4 / Fxra and Nr2a1 / Hnf4a cycled similarly albeit with a lesser amplitude (Figure 3). In most cases, a time-restricted feeding regimen increased the amplitude of oscillations, without altering the phase (right panels), in line with a recent report (Deota et al, 2023). More surprisingly, several NRs exhibited condition-specific cycling (ad libitum-fed: Nr4a2 / Nurr1, Nr5a2 / Lrh1, Nr1f1 / Rora, Nr3c2 / Mr, Nr1i2 / Pxr, Nr1c3 / Pparg ; time-restricted feeding: Nr2b3 / Rxrg, Nr1h2 / Lxrb, Nr3c1 / Gr, Nr1h3 / Lxra, Nr2b2 / Rxrb, Nr1i3 / Car ).…”

Section: Resultssupporting

confidence: 90%

Section: Circadian Rhythmicity Of Hepatic Nuclear Receptors Expressionsupporting

confidence: 90%

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A time- and space-resolved nuclear receptor atlas in mouse liver

Zummo

Berthier

Gheeraert

et al. 2023

Preprint

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The unique functional versatility of the liver is paramount for organismal homeostasis. Both liver development and adult functions are controlled by tightly regulated transcription factor networks, within which nuclear receptors (NRs) regulate essential functions of parenchymal and non-parenchymal cells. Acting as transcription factors sensitive to extracellular cues such as steroidal hormones, lipid metabolites and xenobiotics and modulated by intracellular signaling pathways, NRs orchestrate many aspects of hepatic physiology. While liver functional zonation and adaptability to fluctuating conditions are known to rely on a sophisticated cellular architecture, a comprehensive knowledge of NRs functions in the different liver cell types is still lacking. As a first step toward the accurate mapping of NR functions in mouse liver, we characterized their levels of expression in whole liver as a function of time and diet, and explored NRs isoform expression in hepatocytes, cholangiocytes, Kupffer cells, hepatic stellate cells and liver sinusoidal cells. In addition, we leveraged liver single cell RNAseq studies to provide here an up-to-date compendium of NR expression in mouse liver in space and time.

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Section: Resultssupporting

confidence: 90%

Section: Circadian Rhythmicity Of Hepatic Nuclear Receptors Expressionsupporting

confidence: 90%

A time- and space-resolved nuclear receptor atlas in mouse liver

Zummo

Berthier

Gheeraert

et al. 2023

Preprint

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“…Recently, Deota et al speculated that the rhythmicity of output gene expression in most tissues is not exclusively driven by the circadian clock. Systemic signals generated by other factors (e.g., feeding-fasting cycles) combined with endogenous clock modulated signals may play a dominant role in regulating the rhythmicity of gene expression in peripheral organs ( 56 ). Therefore, further exploration of the mechanisms by which HFD leads to decoupling the core clock from the downstream core clock-controlled output system is potentially valuable for addressing the pathophysiological alterations in the structure and function of MGs caused by HFD.…”

Section: Discussionmentioning

confidence: 99%

High-fat intake reshapes the circadian transcriptome profile and metabolism in murine meibomian glands

Zou

Liu

et al. 2023

Front. Nutr.

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BackgroundNutritional and food components reshape the peripheral clock and metabolism. However, whether food challenges affect the circadian clock and metabolism of meibomian glands (MGs) has not been fully explored. This study was designed to analyze alterations in the rhythmic transcriptome and metabolism of MGs of murine fed a balanced diet or a high-fat diet (HFD).MethodsMale C57BL/6J mice were maintained on a 12/12 h light/dark cycle and fed ad libitum on normal chow (NC) or HFD for 4 weeks. MGs were collected from sacrificed animals at 3-h intervals throughout a 24-h circadian cycle. The circadian transcriptome of MGs was analyzed via bioinformatics approaches using high-throughput RNA sequencing (RNA-seq). In addition, circadian oscillations of lipid components in MGs were analyzed.ResultsMeibomian glands displayed robust transcriptome rhythmicity. HFD feeding significantly altered the circadian transcriptome profile of MGs—including composition and phase—and spatiotemporally affected the enriched signaling pathways. In addition, HFD feeding significantly altered the normal rhythmic oscillations of lipid components in MGs.ConclusionOur data show that HFD significantly affects MGs’ rhythmicity, which reveals a high sensitivity of MGs’ clocks to lipid composition in food.

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“…Although our results indicate that RF might prevent or reduce inflammation by activating the intestinal clock, this is particularly difficult to prove due to the circadian system-wide effects of RF. Namely, RF was found to induce phase shifts in clock gene expression in the liver, kidney, pancreas, WAT and intestinal tissue 69, 70 and to affect gene expression involved in inflammatory signalling such as NF-kB, TLR or IL-17 in many tissues including the intestine 71 . Here, we provide the first direct mechanistic evidence that the effect of RF on the severity of IBD is gated by the intestinal clock, because RF failed to reduce the inflammatory phenotype (immune cells infiltration, inflammatory marker gene expression, histopathological scores) due to genetic dysfunction of the intestinal clock in Bmal1 IEC-/- x IL-10 -/- mice.…”

Section: Discussionmentioning

confidence: 99%

Targeting the intestinal circadian clock by meal timing ameliorates gastrointestinal inflammation

Niu

Heddes

Altaha

et al. 2023

Preprint

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Objective: Impaired clock genes expression has been observed in biopsy samples from patients with inflammatory bowel disease (IBD). Disruption of circadian rhythms, which occurs in shift workers, has been linked to an increased risk of gastrointestinal diseases, including IBD. The intestinal clock balances gastrointestinal homeostasis by regulating the microbiome. Here we characterize intestinal immune functions in mice lacking the intestinal clock and IBD-relevant mouse model under different feeding conditions to describe the functional impact of the intestinal clock in the development of gastrointestinal inflammation. Design: Tissues and fecal samples from intestinal clock-deficient mice (Bmal1IEC-/-) and mouse models for colitis (IL-10-/-, Bmal1IEC-/-xIL-10-/-, dextran sulfate sodium (DSS) administration) under ad libitum and restricted feeding (RF) conditions were used to determine the causal role of the intestinal clock for colitis. Results: In IL-10-/- mice, inflammation correlated with disrupted colon clock genes expression. Genetic loss of intestinal clock functions promoted DSS and IBD inflammatory phenotypes and dramatically reduces survival, and colonization with disease-associated microbiota in germ-free Bmal1IEC-/- hosts increased their inflammatory responses, demonstrating the causal role of colonic clock disruption and the severity of IBD. RF in IL-10-/- mice restored the colon clock and related immune functions, improved the inflammatory responses and rescued the histopathological phenotype. In contrast, RF failed to improve IBD symptoms in Bmal1IEC-/-xIL-10-/- demonstrating the significance of the colonic clock to gate the effect of RF. Conclusion: We provide evidence that inflammation-associated intestinal clock dysfunction triggers host immune imbalance and promotes the development and progression of IBD-like colitis. Enhancing intestinal clock function by RF modulates the pathogenesis of IBD and thus could become a novel strategy to ameliorate the symptoms in IBD patients.

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Diurnal transcriptome landscape of a multi-tissue response to time-restricted feeding in mammals

Cited by 57 publications

References 78 publications

A time- and space-resolved nuclear receptor atlas in mouse liver

A time- and space-resolved nuclear receptor atlas in mouse liver

High-fat intake reshapes the circadian transcriptome profile and metabolism in murine meibomian glands

Targeting the intestinal circadian clock by meal timing ameliorates gastrointestinal inflammation

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