Di Luccia Blanda, Massis Liliana M, Butler Daniel S C, Narasimhan Ramya, Ruddle Sarah J, Pham Trung H M, Vilches-Moure José G, Monack Denise M
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA.
Department of Cellular Microbiology, Max Planck Institute for Infection Biology, Berlin, Germany.
J Exp Med. 2025 Nov 3;222(11). doi: 10.1084/jem.20242431. Epub 2025 Sep 9.
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.
抵抗,即宿主清除入侵微生物;耐受,即宿主无症状地携带高病原体负荷。在此,我们研究了沙门氏菌超级传播者(SSP)宿主在慢性感染期间维持无症状状态的机制。我们发现调节性T细胞(Tregs)对于这种疾病耐受状态至关重要,它限制肠道免疫病理学,使SSP宿主得以茁壮成长,同时促进沙门氏菌传播。SSP小鼠体内Treg的缺失导致存活率降低、肠道炎症加剧以及肠道屏障受损,但不影响沙门氏菌的持续存在。来自SSP小鼠的结肠Tregs表现出独特的转录组特征,其特征是1型炎症基因上调,包括转录因子T-bet。在没有Tregs的情况下,我们观察到细胞毒性CD4+ T细胞的强劲扩增,而CD4+ T细胞的缺失恢复了体内平衡。这些结果揭示了慢性肠道感染期间建立疾病耐受的关键宿主策略,为黏膜对持续性病原体和慢性肠道炎症的反应提供了新的见解。