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Salmonella-superspreader hosts require gut regulatory T cells to maintain a disease-tolerant state

Di Luccia, Blanda ; Massis, Liliana M. ; Butler, Daniel S.C. LU ; Narasimhan, Ramya ; Ruddle, Sarah J. ; Pham, Trung H.M. ; Vilches-Moure, José G. and Monack, Denise M. (2025) In The Journal of experimental medicine 222(11). p.1-17
Abstract

Host-pathogen interactions involve two critical strategies: resistance, whereby hosts clear invading microbes, and tolerance, whereby hosts carry high pathogen burden asymptomatically. Here, we investigate mechanisms by which Salmonella-superspreader (SSP) hosts maintain an asymptomatic state during chronic infection. We found that regulatory T cells (Tregs) are essential for this disease-tolerant state, limiting intestinal immunopathology and enabling SSP hosts to thrive, while facilitating Salmonella transmission. Treg depletion in SSP mice resulted in decreased survival, heightened gut inflammation, and impairment of the intestinal barrier, without affecting Salmonella persistence. Colonic Tregs from SSP mice exhibited a unique... (More)

Host-pathogen interactions involve two critical strategies: resistance, whereby hosts clear invading microbes, and tolerance, whereby hosts carry high pathogen burden asymptomatically. Here, we investigate mechanisms by which Salmonella-superspreader (SSP) hosts maintain an asymptomatic state during chronic infection. We found that regulatory T cells (Tregs) are essential for this disease-tolerant state, limiting intestinal immunopathology and enabling SSP hosts to thrive, while facilitating Salmonella transmission. Treg depletion in SSP mice resulted in decreased survival, heightened gut inflammation, and impairment of the intestinal barrier, without affecting Salmonella persistence. Colonic Tregs from SSP mice exhibited a unique transcriptomic profile characterized by the upregulation of type 1 inflammatory genes, including the transcription factor T-bet. In the absence of Tregs, we observed robust expansion of cytotoxic CD4+ T cells, with CD4+ T cell depletion restoring homeostasis. These results uncover a critical host strategy to establish disease tolerance during chronic enteric infection, providing novel insights into mucosal responses to persistent pathogens and chronic intestinal inflammation.

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author
; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
in
The Journal of experimental medicine
volume
222
issue
11
article number
e20242431
pages
1 - 17
publisher
Rockefeller University Press
external identifiers
  • scopus:105015484461
  • pmid:40924026
ISSN
1540-9538
DOI
10.1084/jem.20242431
language
English
LU publication?
no
additional info
Publisher Copyright: © 2025 Di Luccia et al.
id
35743310-5af9-4c3c-974e-88a3ec69f2dc
date added to LUP
2026-09-09 15:42:10
date last changed
2026-09-10 08:16:33
@article{35743310-5af9-4c3c-974e-88a3ec69f2dc,
  abstract     = {{<p>Host-pathogen interactions involve two critical strategies: resistance, whereby hosts clear invading microbes, and tolerance, whereby hosts carry high pathogen burden asymptomatically. Here, we investigate mechanisms by which Salmonella-superspreader (SSP) hosts maintain an asymptomatic state during chronic infection. We found that regulatory T cells (Tregs) are essential for this disease-tolerant state, limiting intestinal immunopathology and enabling SSP hosts to thrive, while facilitating Salmonella transmission. Treg depletion in SSP mice resulted in decreased survival, heightened gut inflammation, and impairment of the intestinal barrier, without affecting Salmonella persistence. Colonic Tregs from SSP mice exhibited a unique transcriptomic profile characterized by the upregulation of type 1 inflammatory genes, including the transcription factor T-bet. In the absence of Tregs, we observed robust expansion of cytotoxic CD4+ T cells, with CD4+ T cell depletion restoring homeostasis. These results uncover a critical host strategy to establish disease tolerance during chronic enteric infection, providing novel insights into mucosal responses to persistent pathogens and chronic intestinal inflammation.</p>}},
  author       = {{Di Luccia, Blanda and Massis, Liliana M. and Butler, Daniel S.C. and Narasimhan, Ramya and Ruddle, Sarah J. and Pham, Trung H.M. and Vilches-Moure, José G. and Monack, Denise M.}},
  issn         = {{1540-9538}},
  language     = {{eng}},
  month        = {{11}},
  number       = {{11}},
  pages        = {{1--17}},
  publisher    = {{Rockefeller University Press}},
  series       = {{The Journal of experimental medicine}},
  title        = {{Salmonella-superspreader hosts require gut regulatory T cells to maintain a disease-tolerant state}},
  url          = {{http://dx.doi.org/10.1084/jem.20242431}},
  doi          = {{10.1084/jem.20242431}},
  volume       = {{222}},
  year         = {{2025}},
}