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Identification of tonsillar CD4 + CD25 - LAG3 + T cells as naturally occurring IL-10-producing regulatory T cells in human lymphoid tissue

Shuji Sumitomo, Shinichiro Nakachi, Tomohisa Okamura, Yumi Tsuchida, Rika Kato, Hirofumi Shoda, Asayo Furukawa, Nobuo Kitahara, Kenji Kondo, Tatsuya Yamasoba, Kazuhiko Yamamoto, Keishi Fujio
Journal of Autoimmunity 2017, 76: 75-84
IL-10-producing regulatory T cells (IL-10-producing Tregs) are one of the regulatory T cell subsets characterized by the production of high amounts of IL-10, the lack of FOXP3 expression and the strong immunosuppressive capabilities. IL-10-producing Tregs have been primarily reported as induced populations thus far, in part because identifying naturally occurring IL-10-producing Tregs was difficult due to the lack of definitive surface markers. Lymphocyte-activation gene 3 (LAG3) is a CD4 homologue that we have identified as being expressed on IL-10 producing Tregs. In human PBMC, LAG3 combined with CD49b efficiently identifies IL-10-producing Tregs. However, naturally occurring IL-10-producing Tregs in human secondary lymphoid tissue have not been described. In this report, we identified CD4+ CD25- LAG3+ T cells in human tonsil. This T cell subset produced high amounts of IL-10 and expressed low levels of FOXP3. Surface markers and microarray analysis revealed that this is a distinct tonsillar CD4+ T cell subset. CD4+ CD25- LAG3+ T cells expressed interleukin 10 (IL10), PR/SET domain 1 (PRDM1), and CD274 at high levels and chemokine receptor 5 (CXCR5) at low levels. CD4+ CD25- LAG3+ T cells suppressed antibody production more efficiently than CD4+ CD25+ T cells, and CD4+ CD25- LAG3+ T cells induced B cell apoptosis. Moreover, analysis of humanized mice revealed that this cell subset suppressed a graft-versus-host disease (GVHD) reaction in vivo. Our study reveals the existence of naturally occurring IL-10-producing Tregs in human secondary lymphoid tissue and their function in immune regulation.


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