Chemical Interplay Between Gut Microbiota and Epigenetics: Implications in Circadian Biology

Overview

Journal Cell Chem Biol

Publisher Cell Press

Specialty Biochemistry

Date 2024 May 22

PMID 38776923

Authors

Samskrathi Aravinda Sharma

Sarah Olanrewaju Oladejo

Zheng Kuang

Affiliations

Soon will be listed here.

Abstract

Circadian rhythms are intrinsic molecular mechanisms that synchronize biological functions with the day/night cycle. The mammalian gut is colonized by a myriad of microbes, collectively named the gut microbiota. The microbiota impacts host physiology via metabolites and structural components. A key mechanism is the modulation of host epigenetic pathways, especially histone modifications. An increasing number of studies indicate the role of the microbiota in regulating host circadian rhythms. However, the mechanisms remain largely unknown. Here, we summarize studies on microbial regulation of host circadian rhythms and epigenetic pathways, highlight recent findings on how the microbiota employs host epigenetic machinery to regulate circadian rhythms, and discuss its impacts on host physiology, particularly immune and metabolic functions. We further describe current challenges and resources that could facilitate research on microbiota-epigenetic-circadian rhythm interactions to advance our knowledge of circadian disorders and possible therapeutic avenues.

Citing Articles

The evolving understanding of systemic mechanisms in organ-specific IgA nephropathy: a focus on gut-kidney crosstalk.

Wang X, Zhou X, Qiao X, Falchi M, Liu J, Zhang H Theranostics. 2025; 15(2):656-681.

PMID: 39744688 PMC: 11671385. DOI: 10.7150/thno.104631.

Evaluating diurnal rhythms of host responses to enteric norovirus infection in mouse models.

Zhang J, Orchard R, Kuang Z Immunometabolism (Cobham). 2024; 6(4):e00052.

PMID: 39634021 PMC: 11614453. DOI: 10.1097/IN9.0000000000000052.

Sleep and Immune System Crosstalk: Implications for Inflammatory Homeostasis and Disease Pathogenesis.

Singh K, Ghosh S, Bhola A, Verma P, Amist A, Sharma H Ann Neurosci. 2024; :09727531241275347.

PMID: 39544655 PMC: 11559494. DOI: 10.1177/09727531241275347.

References

Tahara Y, Yamazaki M, Sukigara H, Motohashi H, Sasaki H, Miyakawa H . Gut Microbiota-Derived Short Chain Fatty Acids Induce Circadian Clock Entrainment in Mouse Peripheral Tissue. Sci Rep. 2018; 8(1):1395. PMC: 5780501. DOI: 10.1038/s41598-018-19836-7. View

Bijnens S, Depoortere I . Controlled light exposure and intermittent fasting as treatment strategies for metabolic syndrome and gut microbiome dysregulation in night shift workers. Physiol Behav. 2023; 263:114103. DOI: 10.1016/j.physbeh.2023.114103. View

Reddy A, Rey G . Metabolic and nontranscriptional circadian clocks: eukaryotes. Annu Rev Biochem. 2014; 83:165-89. PMC: 4768355. DOI: 10.1146/annurev-biochem-060713-035623. View

Ehichioya D, Taufique S, Magana I, Farah S, Obata Y, Yamazaki S . Gut microbiota depletion minimally affects the daily voluntary wheel running activity and food anticipatory activity in female and male C57BL/6J mice. Front Physiol. 2023; 14:1299474. PMC: 10722266. DOI: 10.3389/fphys.2023.1299474. View

Yang W, Yu T, Huang X, Bilotta A, Xu L, Lu Y . Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020; 11(1):4457. PMC: 7478978. DOI: 10.1038/s41467-020-18262-6. View

Li Q, Wang B, Qiu H, Yan X, Cheng L, Wang Q . Chronic Jet Lag Exacerbates Jejunal and Colonic Microenvironment in Mice. Front Cell Infect Microbiol. 2021; 11:648175. PMC: 8204051. DOI: 10.3389/fcimb.2021.648175. View

Zhao Y, Garcia B . Comprehensive Catalog of Currently Documented Histone Modifications. Cold Spring Harb Perspect Biol. 2015; 7(9):a025064. PMC: 4563710. DOI: 10.1101/cshperspect.a025064. View

Nussbaum J, Van Dyken S, von Moltke J, Cheng L, Mohapatra A, Molofsky A . Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013; 502(7470):245-8. PMC: 3795960. DOI: 10.1038/nature12526. View

Hooper L, Gordon J . Commensal host-bacterial relationships in the gut. Science. 2001; 292(5519):1115-8. DOI: 10.1126/science.1058709. View

10.

Gupta M, Han J, Stenson M, Wellik L, Witzig T . Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia. 2011; 26(6):1356-64. PMC: 3625618. DOI: 10.1038/leu.2011.340. View

11.

Crosio C, Cermakian N, Allis C, Sassone-Corsi P . Light induces chromatin modification in cells of the mammalian circadian clock. Nat Neurosci. 2000; 3(12):1241-7. DOI: 10.1038/81767. View

12.

Choi H, Rao M, Chang E . Gut microbiota as a transducer of dietary cues to regulate host circadian rhythms and metabolism. Nat Rev Gastroenterol Hepatol. 2021; 18(10):679-689. PMC: 8521648. DOI: 10.1038/s41575-021-00452-2. View

13.

Duong H, Robles M, Knutti D, Weitz C . A molecular mechanism for circadian clock negative feedback. Science. 2011; 332(6036):1436-9. PMC: 3859310. DOI: 10.1126/science.1196766. View

14.

Bishehsari F, Voigt R, Keshavarzian A . Circadian rhythms and the gut microbiota: from the metabolic syndrome to cancer. Nat Rev Endocrinol. 2020; 16(12):731-739. PMC: 8085809. DOI: 10.1038/s41574-020-00427-4. View

15.

Desmet L, Thijs T, Mas R, Verbeke K, Depoortere I . Time-Restricted Feeding in Mice Prevents the Disruption of the Peripheral Circadian Clocks and Its Metabolic Impact during Chronic Jetlag. Nutrients. 2021; 13(11). PMC: 8622682. DOI: 10.3390/nu13113846. View

16.

Qin Y, Roberts J, Grimm S, Lih F, Deterding L, Li R . An obesity-associated gut microbiome reprograms the intestinal epigenome and leads to altered colonic gene expression. Genome Biol. 2018; 19(1):7. PMC: 5782396. DOI: 10.1186/s13059-018-1389-1. View

17.

Kelly D, Kotliar M, Woo V, Jagannathan S, Whitt J, Moncivaiz J . Microbiota-sensitive epigenetic signature predicts inflammation in Crohn's disease. JCI Insight. 2018; 3(18). PMC: 6237229. DOI: 10.1172/jci.insight.122104. View

18.

Chang P, Hao L, Offermanns S, Medzhitov R . The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014; 111(6):2247-52. PMC: 3926023. DOI: 10.1073/pnas.1322269111. View

19.

Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D . The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 2008; 134(2):329-40. PMC: 3526943. DOI: 10.1016/j.cell.2008.07.002. View

20.

Vdovikova S, Gilfillan S, Wang S, Dongre M, Nyunt Wai S, Hurtado A . Modulation of gene transcription and epigenetics of colon carcinoma cells by bacterial membrane vesicles. Sci Rep. 2018; 8(1):7434. PMC: 5943334. DOI: 10.1038/s41598-018-25308-9. View