Salmonella infection accelerates postnatal maturation of the intestinal epithelium

Proc Natl Acad Sci U S A. 2025 Jan 7;122(1):e2403344122. doi: 10.1073/pnas.2403344122. Epub 2024 Dec 30.

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.

Keywords: Salmonella Typhimurium; neonate; postnatal tissue maturation; small intestinal epithelium.

MeSH terms

  • Animals
  • Animals, Newborn
  • Cytokines / metabolism
  • Enterocytes / metabolism
  • Enterocytes / microbiology
  • Interleukin-22
  • Interleukins / metabolism
  • Intestinal Mucosa* / immunology
  • Intestinal Mucosa* / metabolism
  • Intestinal Mucosa* / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Differentiation Factor 88* / genetics
  • Myeloid Differentiation Factor 88* / metabolism
  • Organoids / microbiology
  • Salmonella Infections* / immunology
  • Salmonella Infections* / microbiology
  • Salmonella typhimurium* / growth & development

Substances

  • Myeloid Differentiation Factor 88
  • Cytokines
  • Myd88 protein, mouse
  • Interleukin-22
  • Interleukins