<i>Salmonella</i> infection accelerates postnatal maturation of the intestinal epithelium

S Stefan Schlößer (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) A Anna-Lena Ullrich (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) N Nastaran Fazel Modares (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) M Matthias A. Schmitz (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) J Johannes Schöneich (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) K Kaiyi Zhang (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) I Isabel Richter (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) L Laura Robrahn (Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) S Sarah Schraven (Institute for Experimental Molecular Imaging, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) J James S. Nagai (Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) S Sven-Bastiaan Haange (Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung) S Susan A. V. Jennings (Functional Microbiome Research Group, Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) T Thomas Clavel (Functional Microbiome Research Group, Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) U Ulrike Rolle-Kampczyk (Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung) F Fabian Kiessling (Institute for Experimental Molecular Imaging, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) I Ivan G. Costa (Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) V Vanesa Muncan (Department of Gastroenterology and Hepatology, Tytgat Institute for Intestinal and Liver Research, Amsterdam Gastroenterology Endocrinology and Metabolism, Amsterdam UMC University of Amsterdam) U Urska Repnik (Central Microscopy Facility, University of Kiel) M Martin von Bergen (Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung) A Aline Dupont (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital) M Mathias W. Hornef (Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital)

Abstract

Postnatal establishment of enteric metabolic, host–microbial and immune homeostasis is the result of precisely timed and tightly regulated developmental and adaptive processes. Here, we show that infection with the invasive enteropathogen Salmonella Typhimurium results in accelerated maturation of the neonatal epithelium with premature appearance of antimicrobial, metabolic, developmental, and regenerative features of the adult tissue. Using conditional Myd88-deficient mice, we identify the critical contribution of immune cell-derived mediators. Cytokine stimulation of neonatal intestinal epithelial stem cell organoids suggests a network of synergistic and antagonistic cytokine effects with a significant contribution of IL-22, IL-4/IL-13, TNF, and IL-6 to infection-induced enterocyte reprogramming. Our findings demonstrate that the infection-associated immune cell activation disrupts physiological postnatal tissue maturation and may thereby worsen clinical outcomes and alter the neonatal-adult transition.

Article Details

Volume / Issue Vol. 122, Issue 1
Published January 07, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (21)

S

Stefan Schlößer

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

A

Anna-Lena Ullrich

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

N

Nastaran Fazel Modares

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

M

Matthias A. Schmitz

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

J

Johannes Schöneich

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

K

Kaiyi Zhang

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

I

Isabel Richter

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

L

Laura Robrahn

Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

S

Sarah Schraven

Institute for Experimental Molecular Imaging, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

J

James S. Nagai

Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

S

Sven-Bastiaan Haange

Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung

S

Susan A. V. Jennings

Functional Microbiome Research Group, Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

T

Thomas Clavel

Functional Microbiome Research Group, Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

U

Ulrike Rolle-Kampczyk

Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung

F

Fabian Kiessling

Institute for Experimental Molecular Imaging, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

I

Ivan G. Costa

Institute for Computational Genomics, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

V

Vanesa Muncan

Department of Gastroenterology and Hepatology, Tytgat Institute for Intestinal and Liver Research, Amsterdam Gastroenterology Endocrinology and Metabolism, Amsterdam UMC University of Amsterdam

U

Urska Repnik

Central Microscopy Facility, University of Kiel

M

Martin von Bergen

Department of Molecular Toxicology, Helmholtz-Centre for Environmental Research GmbH—Helmholtz-Zentrum für Umweltforschung

A

Aline Dupont

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital

M

Mathias W. Hornef

Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule Aachen University Hospital