Ayumi Kuratani, Masaaki Okamoto, Sekar Arumsari, Takashi Kobayashi, Miwa Sasai, Masahiro Yamamoto
Regulatory T cells (Tregs) within the tumor microenvironment (TME) exhibit functional heterogeneity, including a Foxp3 + T-bet + subset known as Th1-type Treg (Th1-Treg) cells that exert potent immunosuppressive activity. Although IFN-γ signaling is essential for Th1-Treg differentiation, the cellular source of IFN-γ in tumors has remained unclear. Here, we reveal that Treg cells themselves are one source of IFN-γ, which enhances the Th1-Treg induction. Treg-derived IFN-γ acts in an autocrine manner to stabilize T-bet expression and maintain the Th1-Treg phenotype, while Arg1 + tumor-associated macrophage (TAM)–derived platelet factor 4 (PF4) amplifies this loop by inducing Ifng transcription in Tregs. Conditional deletion of Ifng in Foxp3 + cells impaired Th1-Treg differentiation both in tumors and in the spleen, indicating that Treg-derived IFN-γ contributes to Th1-Treg maintenance at local and systemic levels. Moreover, Treg-derived IFN-γ similarly promoted Th1-Treg generation during experimental autoimmune encephalomyelitis, suggesting its role in type 1 inflammatory environments. Together, these findings reveal that Treg-derived IFN-γ contributes to a positive feedback circuit, acting in concert with other IFN-γ sources and TAM-derived PF4 to sustain Th1-Treg differentiation and accumulation in tumors, thereby reinforcing immunosuppression.