T-bet and RORα control lymph node formation by regulating embryonic innate lymphoid cell differentiation

Nat Immunol. 2021 Oct;22(10):1231-1244. doi: 10.1038/s41590-021-01029-6. Epub 2021 Sep 23.

Abstract

The generation of lymphoid tissues during embryogenesis relies on group 3 innate lymphoid cells (ILC3) displaying lymphoid tissue inducer (LTi) activity and expressing the master transcription factor RORγt. Accordingly, RORγt-deficient mice lack ILC3 and lymphoid structures, including lymph nodes (LN). Whereas T-bet affects differentiation and functions of ILC3 postnatally, the role of T-bet in regulating fetal ILC3 and LN formation remains completely unknown. Using multiple mouse models and single-cell analyses of fetal ILCs and ILC progenitors (ILCP), here we identify a key role for T-bet during embryogenesis and show that its deficiency rescues LN formation in RORγt-deficient mice. Mechanistically, T-bet deletion skews the differentiation fate of fetal ILCs and promotes the accumulation of PLZFhi ILCP expressing central LTi molecules in a RORα-dependent fashion. Our data unveil an unexpected role for T-bet and RORα during embryonic ILC function and highlight that RORγt is crucial in counteracting the suppressive effects of T-bet.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / immunology*
  • Cell Lineage / immunology
  • Female
  • Immunity, Innate / immunology*
  • Lymph Nodes / immunology*
  • Lymphocytes / immunology*
  • Lymphoid Tissue / immunology
  • Mice
  • Nuclear Receptor Subfamily 1, Group F, Member 1 / immunology*
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / immunology
  • T-Box Domain Proteins / immunology*
  • T-Lymphocytes, Helper-Inducer / immunology

Substances

  • Nuclear Receptor Subfamily 1, Group F, Member 1
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • T-Box Domain Proteins
  • T-box transcription factor TBX21