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Short-term dietary changes can result in mucosal and systemic immune depression

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Short-term dietary changes can result in mucosal and systemic immune depression. / Siracusa, Francesco; Schaltenberg, Nicola; Kumar, Yogesh; Lesker, Till R; Steglich, Babett; Liwinski, Timur; Cortesi, Filippo; Frommann, Laura; Diercks, Björn-Phillip; Bönisch, Friedericke; Fischer, Alexander W; Scognamiglio, Pasquale; Pauly, Mira J; Casar, Christian; Cohen, Yotam; Pelczar, Penelope; Agalioti, Theodora; Delfs, Flemming; Worthmann, Anna; Wahib, Ramez; Jagemann, Bettina; Mittrücker, Hans-Willi; Kretz, Oliver; Guse, Andreas H; Izbicki, Jakob R; Lassen, Kara G; Strowig, Till; Schweizer, Michaela; Villablanca, Eduardo J; Elinav, Eran; Huber, Samuel; Heeren, Joerg; Gagliani, Nicola.

in: NAT IMMUNOL, Jahrgang 24, Nr. 9, 09.2023, S. 1473-1486.

Publikationen: SCORING: Beitrag in Fachzeitschrift/Zeitung › SCORING: Zeitschriftenaufsatz › Forschung › Begutachtung

Harvard

Siracusa, F, Schaltenberg, N, Kumar, Y, Lesker, TR, Steglich, B, Liwinski, T, Cortesi, F, Frommann, L, Diercks, B-P, Bönisch, F, Fischer, AW, Scognamiglio, P, Pauly, MJ, Casar, C, Cohen, Y, Pelczar, P, Agalioti, T, Delfs, F, Worthmann, A, Wahib, R, Jagemann, B, Mittrücker, H-W, Kretz, O, Guse, AH, Izbicki, JR, Lassen, KG, Strowig, T, Schweizer, M, Villablanca, EJ, Elinav, E, Huber, S, Heeren, J & Gagliani, N 2023, 'Short-term dietary changes can result in mucosal and systemic immune depression', NAT IMMUNOL, Jg. 24, Nr. 9, S. 1473-1486. https://doi.org/10.1038/s41590-023-01587-x

APA

Siracusa, F., Schaltenberg, N., Kumar, Y., Lesker, T. R., Steglich, B., Liwinski, T., Cortesi, F., Frommann, L., Diercks, B-P., Bönisch, F., Fischer, A. W., Scognamiglio, P., Pauly, M. J., Casar, C., Cohen, Y., Pelczar, P., Agalioti, T., Delfs, F., Worthmann, A., ... Gagliani, N. (2023). Short-term dietary changes can result in mucosal and systemic immune depression. NAT IMMUNOL, 24(9), 1473-1486. https://doi.org/10.1038/s41590-023-01587-x

Vancouver

Siracusa F, Schaltenberg N, Kumar Y, Lesker TR, Steglich B, Liwinski T et al. Short-term dietary changes can result in mucosal and systemic immune depression. NAT IMMUNOL. 2023 Sep;24(9):1473-1486. https://doi.org/10.1038/s41590-023-01587-x

Bibtex

@article{e84e410ff37b416a87e37cef69e3e775,
title = "Short-term dietary changes can result in mucosal and systemic immune depression",
abstract = "Omnivorous animals, including mice and humans, tend to prefer energy-dense nutrients rich in fat over plant-based diets, especially for short periods of time, but the health consequences of this short-term consumption of energy-dense nutrients are unclear. Here, we show that short-term reiterative switching to 'feast diets', mimicking our social eating behavior, breaches the potential buffering effect of the intestinal microbiota and reorganizes the immunological architecture of mucosa-associated lymphoid tissues. The first dietary switch was sufficient to induce transient mucosal immune depression and suppress systemic immunity, leading to higher susceptibility to Salmonella enterica serovar Typhimurium and Listeria monocytogenes infections. The ability to respond to antigenic challenges with a model antigen was also impaired. These observations could be explained by a reduction of CD4+ T cell metabolic fitness and cytokine production due to impaired mTOR activity in response to reduced microbial provision of fiber metabolites. Reintroducing dietary fiber rewired T cell metabolism and restored mucosal and systemic CD4+ T cell functions and immunity. Finally, dietary intervention with human volunteers confirmed the effect of short-term dietary switches on human CD4+ T cell functionality. Therefore, short-term nutritional changes cause a transient depression of mucosal and systemic immunity, creating a window of opportunity for pathogenic infection.",
keywords = "Humans, Mice, Animals, Mucous Membrane, Salmonella typhimurium, T-Lymphocytes, Immunity, Mucosal",
author = "Francesco Siracusa and Nicola Schaltenberg and Yogesh Kumar and Lesker, {Till R} and Babett Steglich and Timur Liwinski and Filippo Cortesi and Laura Frommann and Bj{\"o}rn-Phillip Diercks and Friedericke B{\"o}nisch and Fischer, {Alexander W} and Pasquale Scognamiglio and Pauly, {Mira J} and Christian Casar and Yotam Cohen and Penelope Pelczar and Theodora Agalioti and Flemming Delfs and Anna Worthmann and Ramez Wahib and Bettina Jagemann and Hans-Willi Mittr{\"u}cker and Oliver Kretz and Guse, {Andreas H} and Izbicki, {Jakob R} and Lassen, {Kara G} and Till Strowig and Michaela Schweizer and Villablanca, {Eduardo J} and Eran Elinav and Samuel Huber and Joerg Heeren and Nicola Gagliani",
note = "{\textcopyright} 2023. The Author(s).",
year = "2023",
month = sep,
doi = "10.1038/s41590-023-01587-x",
language = "English",
volume = "24",
pages = "1473--1486",
journal = "NAT IMMUNOL",
issn = "1529-2908",
publisher = "NATURE PUBLISHING GROUP",
number = "9",

}

RIS

TY - JOUR

T1 - Short-term dietary changes can result in mucosal and systemic immune depression

AU - Siracusa, Francesco

AU - Schaltenberg, Nicola

AU - Kumar, Yogesh

AU - Lesker, Till R

AU - Steglich, Babett

AU - Liwinski, Timur

AU - Cortesi, Filippo

AU - Frommann, Laura

AU - Diercks, Björn-Phillip

AU - Bönisch, Friedericke

AU - Fischer, Alexander W

AU - Scognamiglio, Pasquale

AU - Pauly, Mira J

AU - Casar, Christian

AU - Cohen, Yotam

AU - Pelczar, Penelope

AU - Agalioti, Theodora

AU - Delfs, Flemming

AU - Worthmann, Anna

AU - Wahib, Ramez

AU - Jagemann, Bettina

AU - Mittrücker, Hans-Willi

AU - Kretz, Oliver

AU - Guse, Andreas H

AU - Izbicki, Jakob R

AU - Lassen, Kara G

AU - Strowig, Till

AU - Schweizer, Michaela

AU - Villablanca, Eduardo J

AU - Elinav, Eran

AU - Huber, Samuel

AU - Heeren, Joerg

AU - Gagliani, Nicola

N1 - © 2023. The Author(s).

PY - 2023/9

Y1 - 2023/9

N2 - Omnivorous animals, including mice and humans, tend to prefer energy-dense nutrients rich in fat over plant-based diets, especially for short periods of time, but the health consequences of this short-term consumption of energy-dense nutrients are unclear. Here, we show that short-term reiterative switching to 'feast diets', mimicking our social eating behavior, breaches the potential buffering effect of the intestinal microbiota and reorganizes the immunological architecture of mucosa-associated lymphoid tissues. The first dietary switch was sufficient to induce transient mucosal immune depression and suppress systemic immunity, leading to higher susceptibility to Salmonella enterica serovar Typhimurium and Listeria monocytogenes infections. The ability to respond to antigenic challenges with a model antigen was also impaired. These observations could be explained by a reduction of CD4+ T cell metabolic fitness and cytokine production due to impaired mTOR activity in response to reduced microbial provision of fiber metabolites. Reintroducing dietary fiber rewired T cell metabolism and restored mucosal and systemic CD4+ T cell functions and immunity. Finally, dietary intervention with human volunteers confirmed the effect of short-term dietary switches on human CD4+ T cell functionality. Therefore, short-term nutritional changes cause a transient depression of mucosal and systemic immunity, creating a window of opportunity for pathogenic infection.

AB - Omnivorous animals, including mice and humans, tend to prefer energy-dense nutrients rich in fat over plant-based diets, especially for short periods of time, but the health consequences of this short-term consumption of energy-dense nutrients are unclear. Here, we show that short-term reiterative switching to 'feast diets', mimicking our social eating behavior, breaches the potential buffering effect of the intestinal microbiota and reorganizes the immunological architecture of mucosa-associated lymphoid tissues. The first dietary switch was sufficient to induce transient mucosal immune depression and suppress systemic immunity, leading to higher susceptibility to Salmonella enterica serovar Typhimurium and Listeria monocytogenes infections. The ability to respond to antigenic challenges with a model antigen was also impaired. These observations could be explained by a reduction of CD4+ T cell metabolic fitness and cytokine production due to impaired mTOR activity in response to reduced microbial provision of fiber metabolites. Reintroducing dietary fiber rewired T cell metabolism and restored mucosal and systemic CD4+ T cell functions and immunity. Finally, dietary intervention with human volunteers confirmed the effect of short-term dietary switches on human CD4+ T cell functionality. Therefore, short-term nutritional changes cause a transient depression of mucosal and systemic immunity, creating a window of opportunity for pathogenic infection.

KW - Humans

KW - Mice

KW - Animals

KW - Mucous Membrane

KW - Salmonella typhimurium

KW - T-Lymphocytes

KW - Immunity, Mucosal

U2 - 10.1038/s41590-023-01587-x

DO - 10.1038/s41590-023-01587-x

M3 - SCORING: Journal article

C2 - 37580603

VL - 24

SP - 1473

EP - 1486

JO - NAT IMMUNOL

JF - NAT IMMUNOL

SN - 1529-2908

IS - 9

ER -