IL-1β and IL-23 Promote Extrathymic Commitment of CD27+CD122- γδ T Cells to γδT17 Cells

J Immunol. 2017 Oct 15;199(8):2668-2679. doi: 10.4049/jimmunol.1700287. Epub 2017 Aug 30.

Abstract

γδT17 cells are a subset of γδ T cells committed to IL-17 production and are characterized by the expression of IL-23R and CCR6 and lack of CD27 expression. γδT17 cells are believed to arise within a narrow time window during prenatal thymic development. In agreement with this concept, we show in this study that adult Rag1-/- recipient mice of Il23rgfp/+ (IL-23R reporter) bone marrow selectively lack IL-23R+ γδT17 cells. Despite their absence in secondary lymphoid tissues during homeostasis, γδT17 cells emerge in bone marrow chimeric mice upon induction of skin inflammation by topical treatment with imiquimod cream (Aldara). We demonstrate that IL-1β and IL-23 together are able to promote the development of bona fide γδT17 cells from peripheral CD122-IL-23R- γδ T cells, whereas CD122+ γδ T cells fail to convert into γδT17 cells and remain stable IFN-γ producers (γδT1 cells). IL-23 is instrumental in expanding extrathymically generated γδT17 cells. In particular, TCR-Vγ4+ chain-expressing CD122-IL-23R- γδ T cells are induced to express IL-23R and IL-17 outside the thymus during skin inflammation. In contrast, TCR-Vγ1+ γδ T cells largely resist this process because prior TCR engagement in the thymus has initiated their commitment to the γδT1 lineage. In summary, our data reveal that the peripheral pool of γδ T cells retains a considerable degree of plasticity because it harbors "naive" precursors, which can be induced to produce IL-17 and replenish peripheral niches that are usually occupied by thymus-derived γδT17 cells.

MeSH terms

  • Aminoquinolines
  • Animals
  • Cell Differentiation
  • Cells, Cultured
  • Disease Models, Animal
  • Humans
  • Imiquimod
  • Interleukin-17 / metabolism*
  • Interleukin-1beta / metabolism
  • Interleukin-2 Receptor beta Subunit / metabolism
  • Interleukin-23 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Psoriasis / immunology*
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Receptors, Interleukin / genetics
  • T-Lymphocytes / physiology*
  • Tumor Necrosis Factor Receptor Superfamily, Member 7 / metabolism

Substances

  • Aminoquinolines
  • Interleukin-17
  • Interleukin-1beta
  • Interleukin-2 Receptor beta Subunit
  • Interleukin-23
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, Interleukin
  • Tumor Necrosis Factor Receptor Superfamily, Member 7
  • interleukin-23 receptor, mouse
  • Imiquimod