Foxp3 orchestrates reorganization of chromatin architecture to establish regulatory T cell identity

Zhi Liu, Dong-Sung Lee, Yuqiong Liang, Ye Zheng () and Jesse R. Dixon ()
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Zhi Liu: Shanghai Jiao Tong University School of Medicine
Dong-Sung Lee: Salk Institute for Biological Studies
Yuqiong Liang: Salk Institute for Biological Studies
Ye Zheng: Salk Institute for Biological Studies
Jesse R. Dixon: Salk Institute for Biological Studies

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Chromatin conformation reorganization is emerging as an important layer of regulation for gene expression and lineage specification. Yet, how lineage-specific transcription factors contribute to the establishment of cell type-specific 3D chromatin architecture in the immune cells remains unclear, especially for the late stages of T cell subset differentiation and maturation. Regulatory T cells (Treg) are mainly generated in the thymus as a subpopulation of T cells specializing in suppressing excessive immune responses. Here, by comprehensively mapping 3D chromatin organization during Treg cell differentiation, we show that Treg-specific chromatin structures were progressively established during its lineage specification, and highly associated with Treg signature gene expression. Additionally, the binding sites of Foxp3, a Treg lineage specifying transcription factor, were highly enriched at Treg-specific chromatin loop anchors. Further comparison of the chromatin interactions between wide-type Tregs versus Treg cells from Foxp3 knock-in/knockout or newly-generated Foxp3 domain-swap mutant mouse revealed that Foxp3 was essential for the establishment of Treg-specific 3D chromatin architecture, although it was not dependent on the formation of the Foxp3 domain-swapped dimer. These results highlighted an underappreciated role of Foxp3 in modulating Treg-specific 3D chromatin structure formation.

Date: 2023
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DOI: 10.1038/s41467-023-42647-y

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