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Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis

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Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis. / Tuganbaev, Timur; Mor, Uria; Bashiardes, Stavros; Liwinski, Timur; Nobs, Samuel Philip; Leshem, Avner; Dori-Bachash, Mally; Thaiss, Christoph A; Pinker, Elisha Y; Ratiner, Karina; Adlung, Lorenz; Federici, Sara; Kleimeyer, Christian; Moresi, Claudia; Yamada, Takahiro; Cohen, Yotam; Zhang, Xiao; Massalha, Hassan; Massasa, Efi; Kuperman, Yael; Koni, Pandelakis A; Harmelin, Alon; Gao, Nan; Itzkovitz, Shalev; Honda, Kenya; Shapiro, Hagit; Elinav, Eran.

In: CELL, Vol. 182, No. 6, 17.09.2020, p. 1441-1459.e21.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Tuganbaev, T, Mor, U, Bashiardes, S, Liwinski, T, Nobs, SP, Leshem, A, Dori-Bachash, M, Thaiss, CA, Pinker, EY, Ratiner, K, Adlung, L, Federici, S, Kleimeyer, C, Moresi, C, Yamada, T, Cohen, Y, Zhang, X, Massalha, H, Massasa, E, Kuperman, Y, Koni, PA, Harmelin, A, Gao, N, Itzkovitz, S, Honda, K, Shapiro, H & Elinav, E 2020, 'Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis', CELL, vol. 182, no. 6, pp. 1441-1459.e21. https://doi.org/10.1016/j.cell.2020.08.027

APA

Tuganbaev, T., Mor, U., Bashiardes, S., Liwinski, T., Nobs, S. P., Leshem, A., Dori-Bachash, M., Thaiss, C. A., Pinker, E. Y., Ratiner, K., Adlung, L., Federici, S., Kleimeyer, C., Moresi, C., Yamada, T., Cohen, Y., Zhang, X., Massalha, H., Massasa, E., ... Elinav, E. (2020). Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis. CELL, 182(6), 1441-1459.e21. https://doi.org/10.1016/j.cell.2020.08.027

Vancouver

Tuganbaev T, Mor U, Bashiardes S, Liwinski T, Nobs SP, Leshem A et al. Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis. CELL. 2020 Sep 17;182(6):1441-1459.e21. https://doi.org/10.1016/j.cell.2020.08.027

Bibtex

@article{77f27344a8244d19b6d4f3b96ffc55c3,
title = "Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis",
abstract = "Throughout a 24-h period, the small intestine (SI) is exposed to diurnally varying food- and microbiome-derived antigenic burdens but maintains a strict immune homeostasis, which when perturbed in genetically susceptible individuals, may lead to Crohn disease. Herein, we demonstrate that dietary content and rhythmicity regulate the diurnally shifting SI epithelial cell (SIEC) transcriptional landscape through modulation of the SI microbiome. We exemplify this concept with SIEC major histocompatibility complex (MHC) class II, which is diurnally modulated by distinct mucosal-adherent SI commensals, while supporting downstream diurnal activity of intra-epithelial IL-10+ lymphocytes regulating the SI barrier function. Disruption of this diurnally regulated diet-microbiome-MHC class II-IL-10-epithelial barrier axis by circadian clock disarrangement, alterations in feeding time or content, or epithelial-specific MHC class II depletion leads to an extensive microbial product influx, driving Crohn-like enteritis. Collectively, we highlight nutritional features that modulate SI microbiome, immunity, and barrier function and identify dietary, epithelial, and immune checkpoints along this axis to be potentially exploitable in future Crohn disease interventions.",
keywords = "Animals, Anti-Bacterial Agents/pharmacology, Circadian Clocks/physiology, Crohn Disease/immunology, Diet, Epithelial Cells/cytology, Flow Cytometry, Gastrointestinal Microbiome/drug effects, Gene Expression Profiling, Histocompatibility Antigens Class II/genetics, Homeostasis, In Situ Hybridization, Fluorescence, Interleukin-10/metabolism, Intestine, Small/immunology, Lymphocytes, Male, Mice, Mice, Inbred C57BL, Mice, Knockout, Periodicity, T-Lymphocytes/immunology, Transcriptome/genetics",
author = "Timur Tuganbaev and Uria Mor and Stavros Bashiardes and Timur Liwinski and Nobs, {Samuel Philip} and Avner Leshem and Mally Dori-Bachash and Thaiss, {Christoph A} and Pinker, {Elisha Y} and Karina Ratiner and Lorenz Adlung and Sara Federici and Christian Kleimeyer and Claudia Moresi and Takahiro Yamada and Yotam Cohen and Xiao Zhang and Hassan Massalha and Efi Massasa and Yael Kuperman and Koni, {Pandelakis A} and Alon Harmelin and Nan Gao and Shalev Itzkovitz and Kenya Honda and Hagit Shapiro and Eran Elinav",
note = "Copyright {\textcopyright} 2020 Elsevier Inc. All rights reserved.",
year = "2020",
month = sep,
day = "17",
doi = "10.1016/j.cell.2020.08.027",
language = "English",
volume = "182",
pages = "1441--1459.e21",
journal = "CELL",
issn = "0092-8674",
publisher = "Cell Press",
number = "6",

}

RIS

TY - JOUR

T1 - Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis

AU - Tuganbaev, Timur

AU - Mor, Uria

AU - Bashiardes, Stavros

AU - Liwinski, Timur

AU - Nobs, Samuel Philip

AU - Leshem, Avner

AU - Dori-Bachash, Mally

AU - Thaiss, Christoph A

AU - Pinker, Elisha Y

AU - Ratiner, Karina

AU - Adlung, Lorenz

AU - Federici, Sara

AU - Kleimeyer, Christian

AU - Moresi, Claudia

AU - Yamada, Takahiro

AU - Cohen, Yotam

AU - Zhang, Xiao

AU - Massalha, Hassan

AU - Massasa, Efi

AU - Kuperman, Yael

AU - Koni, Pandelakis A

AU - Harmelin, Alon

AU - Gao, Nan

AU - Itzkovitz, Shalev

AU - Honda, Kenya

AU - Shapiro, Hagit

AU - Elinav, Eran

N1 - Copyright © 2020 Elsevier Inc. All rights reserved.

PY - 2020/9/17

Y1 - 2020/9/17

N2 - Throughout a 24-h period, the small intestine (SI) is exposed to diurnally varying food- and microbiome-derived antigenic burdens but maintains a strict immune homeostasis, which when perturbed in genetically susceptible individuals, may lead to Crohn disease. Herein, we demonstrate that dietary content and rhythmicity regulate the diurnally shifting SI epithelial cell (SIEC) transcriptional landscape through modulation of the SI microbiome. We exemplify this concept with SIEC major histocompatibility complex (MHC) class II, which is diurnally modulated by distinct mucosal-adherent SI commensals, while supporting downstream diurnal activity of intra-epithelial IL-10+ lymphocytes regulating the SI barrier function. Disruption of this diurnally regulated diet-microbiome-MHC class II-IL-10-epithelial barrier axis by circadian clock disarrangement, alterations in feeding time or content, or epithelial-specific MHC class II depletion leads to an extensive microbial product influx, driving Crohn-like enteritis. Collectively, we highlight nutritional features that modulate SI microbiome, immunity, and barrier function and identify dietary, epithelial, and immune checkpoints along this axis to be potentially exploitable in future Crohn disease interventions.

AB - Throughout a 24-h period, the small intestine (SI) is exposed to diurnally varying food- and microbiome-derived antigenic burdens but maintains a strict immune homeostasis, which when perturbed in genetically susceptible individuals, may lead to Crohn disease. Herein, we demonstrate that dietary content and rhythmicity regulate the diurnally shifting SI epithelial cell (SIEC) transcriptional landscape through modulation of the SI microbiome. We exemplify this concept with SIEC major histocompatibility complex (MHC) class II, which is diurnally modulated by distinct mucosal-adherent SI commensals, while supporting downstream diurnal activity of intra-epithelial IL-10+ lymphocytes regulating the SI barrier function. Disruption of this diurnally regulated diet-microbiome-MHC class II-IL-10-epithelial barrier axis by circadian clock disarrangement, alterations in feeding time or content, or epithelial-specific MHC class II depletion leads to an extensive microbial product influx, driving Crohn-like enteritis. Collectively, we highlight nutritional features that modulate SI microbiome, immunity, and barrier function and identify dietary, epithelial, and immune checkpoints along this axis to be potentially exploitable in future Crohn disease interventions.

KW - Animals

KW - Anti-Bacterial Agents/pharmacology

KW - Circadian Clocks/physiology

KW - Crohn Disease/immunology

KW - Diet

KW - Epithelial Cells/cytology

KW - Flow Cytometry

KW - Gastrointestinal Microbiome/drug effects

KW - Gene Expression Profiling

KW - Histocompatibility Antigens Class II/genetics

KW - Homeostasis

KW - In Situ Hybridization, Fluorescence

KW - Interleukin-10/metabolism

KW - Intestine, Small/immunology

KW - Lymphocytes

KW - Male

KW - Mice

KW - Mice, Inbred C57BL

KW - Mice, Knockout

KW - Periodicity

KW - T-Lymphocytes/immunology

KW - Transcriptome/genetics

U2 - 10.1016/j.cell.2020.08.027

DO - 10.1016/j.cell.2020.08.027

M3 - SCORING: Journal article

C2 - 32888430

VL - 182

SP - 1441-1459.e21

JO - CELL

JF - CELL

SN - 0092-8674

IS - 6

ER -