Regulatory T Cell-Derived TGF-β1 Controls Multiple Checkpoints Governing Allergy and Autoimmunity

Immunity. 2020 Dec 15;53(6):1202-1214.e6. doi: 10.1016/j.immuni.2020.10.002. Epub 2020 Oct 20.

Abstract

The mechanisms by which regulatory T (Treg) cells differentially control allergic and autoimmune responses remain unclear. We show that Treg cells in food allergy (FA) had decreased expression of transforming growth factor beta 1 (TGF-β1) because of interleukin-4 (IL-4)- and signal transducer and activator of transciription-6 (STAT6)-dependent inhibition of Tgfb1 transcription. These changes were modeled by Treg cell-specific Tgfb1 monoallelic inactivation, which induced allergic dysregulation by impairing microbiota-dependent retinoic acid receptor-related orphan receptor gamma t (ROR-γt)+ Treg cell differentiation. This dysregulation was rescued by treatment with Clostridiales species, which upregulated Tgfb1 expression in Treg cells. Biallelic deficiency precipitated fatal autoimmunity with intense autoantibody production and dysregulated T follicular helper and B cell responses. These results identify a privileged role of Treg cell-derived TGF-β1 in regulating allergy and autoimmunity at distinct checkpoints in a Tgfb1 gene dose- and microbiota-dependent manner.

Keywords: ROR-γt; T follicular helper cells; TGF-β; allergy; autoimmunity; checkpoint; food allergy; mast cells; microbiota; regulatory T cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Animals
  • Autoimmunity / genetics
  • Autoimmunity / immunology*
  • B-Lymphocytes / immunology
  • Cell Differentiation
  • Child
  • Child, Preschool
  • Food Hypersensitivity / immunology
  • Gene Dosage
  • Humans
  • Hypersensitivity / genetics
  • Hypersensitivity / immunology*
  • Immunoglobulin G / immunology
  • Infant
  • Mast Cells / immunology
  • Mice
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • T Follicular Helper Cells / immunology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Transcription, Genetic
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / immunology*
  • Young Adult

Substances

  • Immunoglobulin G
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Transforming Growth Factor beta1