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Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling

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Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling. / Pontarollo, Giulia; Kollar, Bettina; Mann, Amrit; Khuu, My Phung; Kiouptsi, Klytaimnistra; Bayer, Franziska; Brandão, Inês; Zinina, Valeriya V; Hahlbrock, Jennifer; Malinarich, Frano; Mimmler, Maximilian; Bhushan, Sudhanshu; Marini, Federico; Ruf, Wolfram; Belheouane, Meriem; Baines, John F; Endres, Kristina; Reba, Scott M; Raker, Verena K; Deppermann, Carsten; Welsch, Christoph; Bosmann, Markus; Soshnikova, Natalia; Chassaing, Benoit; Bergentall, Mattias; Sommer, Felix; Bäckhed, Fredrik; Reinhardt, Christoph.

In: NAT METAB, Vol. 5, No. 7, 07.2023, p. 1174-1187.

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

Harvard

Pontarollo, G, Kollar, B, Mann, A, Khuu, MP, Kiouptsi, K, Bayer, F, Brandão, I, Zinina, VV, Hahlbrock, J, Malinarich, F, Mimmler, M, Bhushan, S, Marini, F, Ruf, W, Belheouane, M, Baines, JF, Endres, K, Reba, SM, Raker, VK, Deppermann, C, Welsch, C, Bosmann, M, Soshnikova, N, Chassaing, B, Bergentall, M, Sommer, F, Bäckhed, F & Reinhardt, C 2023, 'Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling', NAT METAB, vol. 5, no. 7, pp. 1174-1187. https://doi.org/10.1038/s42255-023-00828-5

APA

Pontarollo, G., Kollar, B., Mann, A., Khuu, M. P., Kiouptsi, K., Bayer, F., Brandão, I., Zinina, V. V., Hahlbrock, J., Malinarich, F., Mimmler, M., Bhushan, S., Marini, F., Ruf, W., Belheouane, M., Baines, J. F., Endres, K., Reba, S. M., Raker, V. K., ... Reinhardt, C. (2023). Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling. NAT METAB, 5(7), 1174-1187. https://doi.org/10.1038/s42255-023-00828-5

Vancouver

Pontarollo G, Kollar B, Mann A, Khuu MP, Kiouptsi K, Bayer F et al. Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling. NAT METAB. 2023 Jul;5(7):1174-1187. https://doi.org/10.1038/s42255-023-00828-5

Bibtex

@article{1cd5759bb5234a1f9b3986e7b3559785,
title = "Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling",
abstract = "The gut microbiota influences intestinal barrier integrity through mechanisms that are incompletely understood. Here we show that the commensal microbiota weakens the intestinal barrier by suppressing epithelial neuropilin-1 (NRP1) and Hedgehog (Hh) signaling. Microbial colonization of germ-free mice dampens signaling of the intestinal Hh pathway through epithelial Toll-like receptor (TLR)-2, resulting in decreased epithelial NRP1 protein levels. Following activation via TLR2/TLR6, epithelial NRP1, a positive-feedback regulator of Hh signaling, is lysosomally degraded. Conversely, elevated epithelial NRP1 levels in germ-free mice are associated with a strengthened gut barrier. Functionally, intestinal epithelial cell-specific Nrp1 deficiency (Nrp1ΔIEC) results in decreased Hh pathway activity and a weakened gut barrier. In addition, Nrp1ΔIEC mice have a reduced density of capillary networks in their small intestinal villus structures. Collectively, our results reveal a role for the commensal microbiota and epithelial NRP1 signaling in the regulation of intestinal barrier function through postnatal control of Hh signaling.",
keywords = "Mice, Animals, Neuropilin-1/metabolism, Hedgehog Proteins/metabolism, Signal Transduction, Epithelial Cells/metabolism, Bacteria/metabolism",
author = "Giulia Pontarollo and Bettina Kollar and Amrit Mann and Khuu, {My Phung} and Klytaimnistra Kiouptsi and Franziska Bayer and In{\^e}s Brand{\~a}o and Zinina, {Valeriya V} and Jennifer Hahlbrock and Frano Malinarich and Maximilian Mimmler and Sudhanshu Bhushan and Federico Marini and Wolfram Ruf and Meriem Belheouane and Baines, {John F} and Kristina Endres and Reba, {Scott M} and Raker, {Verena K} and Carsten Deppermann and Christoph Welsch and Markus Bosmann and Natalia Soshnikova and Benoit Chassaing and Mattias Bergentall and Felix Sommer and Fredrik B{\"a}ckhed and Christoph Reinhardt",
note = "{\textcopyright} 2023. The Author(s).",
year = "2023",
month = jul,
doi = "10.1038/s42255-023-00828-5",
language = "English",
volume = "5",
pages = "1174--1187",
journal = "NAT METAB",
issn = "2522-5812",
publisher = "Springer",
number = "7",

}

RIS

TY - JOUR

T1 - Commensal bacteria weaken the intestinal barrier by suppressing epithelial neuropilin-1 and Hedgehog signaling

AU - Pontarollo, Giulia

AU - Kollar, Bettina

AU - Mann, Amrit

AU - Khuu, My Phung

AU - Kiouptsi, Klytaimnistra

AU - Bayer, Franziska

AU - Brandão, Inês

AU - Zinina, Valeriya V

AU - Hahlbrock, Jennifer

AU - Malinarich, Frano

AU - Mimmler, Maximilian

AU - Bhushan, Sudhanshu

AU - Marini, Federico

AU - Ruf, Wolfram

AU - Belheouane, Meriem

AU - Baines, John F

AU - Endres, Kristina

AU - Reba, Scott M

AU - Raker, Verena K

AU - Deppermann, Carsten

AU - Welsch, Christoph

AU - Bosmann, Markus

AU - Soshnikova, Natalia

AU - Chassaing, Benoit

AU - Bergentall, Mattias

AU - Sommer, Felix

AU - Bäckhed, Fredrik

AU - Reinhardt, Christoph

N1 - © 2023. The Author(s).

PY - 2023/7

Y1 - 2023/7

N2 - The gut microbiota influences intestinal barrier integrity through mechanisms that are incompletely understood. Here we show that the commensal microbiota weakens the intestinal barrier by suppressing epithelial neuropilin-1 (NRP1) and Hedgehog (Hh) signaling. Microbial colonization of germ-free mice dampens signaling of the intestinal Hh pathway through epithelial Toll-like receptor (TLR)-2, resulting in decreased epithelial NRP1 protein levels. Following activation via TLR2/TLR6, epithelial NRP1, a positive-feedback regulator of Hh signaling, is lysosomally degraded. Conversely, elevated epithelial NRP1 levels in germ-free mice are associated with a strengthened gut barrier. Functionally, intestinal epithelial cell-specific Nrp1 deficiency (Nrp1ΔIEC) results in decreased Hh pathway activity and a weakened gut barrier. In addition, Nrp1ΔIEC mice have a reduced density of capillary networks in their small intestinal villus structures. Collectively, our results reveal a role for the commensal microbiota and epithelial NRP1 signaling in the regulation of intestinal barrier function through postnatal control of Hh signaling.

AB - The gut microbiota influences intestinal barrier integrity through mechanisms that are incompletely understood. Here we show that the commensal microbiota weakens the intestinal barrier by suppressing epithelial neuropilin-1 (NRP1) and Hedgehog (Hh) signaling. Microbial colonization of germ-free mice dampens signaling of the intestinal Hh pathway through epithelial Toll-like receptor (TLR)-2, resulting in decreased epithelial NRP1 protein levels. Following activation via TLR2/TLR6, epithelial NRP1, a positive-feedback regulator of Hh signaling, is lysosomally degraded. Conversely, elevated epithelial NRP1 levels in germ-free mice are associated with a strengthened gut barrier. Functionally, intestinal epithelial cell-specific Nrp1 deficiency (Nrp1ΔIEC) results in decreased Hh pathway activity and a weakened gut barrier. In addition, Nrp1ΔIEC mice have a reduced density of capillary networks in their small intestinal villus structures. Collectively, our results reveal a role for the commensal microbiota and epithelial NRP1 signaling in the regulation of intestinal barrier function through postnatal control of Hh signaling.

KW - Mice

KW - Animals

KW - Neuropilin-1/metabolism

KW - Hedgehog Proteins/metabolism

KW - Signal Transduction

KW - Epithelial Cells/metabolism

KW - Bacteria/metabolism

U2 - 10.1038/s42255-023-00828-5

DO - 10.1038/s42255-023-00828-5

M3 - SCORING: Journal article

C2 - 37414930

VL - 5

SP - 1174

EP - 1187

JO - NAT METAB

JF - NAT METAB

SN - 2522-5812

IS - 7

ER -