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Murine regulatory T (Treg) cells in tissues promote tissue homeostasis and regeneration. We sought to identify features that characterize human Treg cells with these functions in healthy tissues. Single-cell chromatin accessibility profiles of murine and human tissue Treg cells defined a conserved, microbiota-independent tissue-repair Treg signature with a prevailing footprint of the transcription factor BATF. This signature, combined with gene expression profiling and TCR fate mapping, identified a population of tissue-like Treg cells in human peripheral blood that expressed BATF, chemokine receptor CCR8 and HLA-DR. Human BATF+CCR8+ Treg cells from normal skin and adipose tissue shared features with nonlymphoid T follicular helper-like (Tfh-like) cells, and induction of a Tfh-like differentiation program in naive human Treg cells partially recapitulated tissue Treg regenerative characteristics, including wound healing potential. Human BATF+CCR8+ Treg cells from healthy tissue share features with tumor-resident Treg cells, highlighting the importance of understanding the context-specific functions of these cells.
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•Comparison of chromatin accessibility between murine und human tissue Treg cells•TCR tracking revealed clonal relationship between tissue and blood BATF+CCR8+ Tregs•Treg cells from healthy tissues were similar to CCR8+ Treg cells from tumors•Tfh-like differentiation program induces tissue Treg cell repair characteristics
Delacher et al. identify a conserved transcriptional and epigenetic signature that defines tissue regulatory T (Treg) cells in mice and humans. BATF+CCR8+ Treg cells from healthy human tissue share features with Treg cells found in tumors, suggesting that characteristics associated with tumor-residency may rather reflect the tissue repair functions of these cells.