SLAM/SAP signaling regulates discrete γδ T cell developmental checkpoints and shapes the innate-like γδ TCR repertoire

Elife. 2024 Dec 10:13:RP97229. doi: 10.7554/eLife.97229.

Abstract

During thymic development, most γδ T cells acquire innate-like characteristics that are critical for their function in tumor surveillance, infectious disease, and tissue repair. The mechanisms, however, that regulate γδ T cell developmental programming remain unclear. Recently, we demonstrated that the SLAM/SAP signaling pathway regulates the development and function of multiple innate-like γδ T cell subsets. Here, we used a single-cell proteogenomics approach to identify SAP-dependent developmental checkpoints and to define the SAP-dependent γδ TCR repertoire in mice. SAP deficiency resulted in both a significant loss of an immature Gzma+Blk+Etv5+Tox2+ γδT17 precursor population and a significant increase in Cd4+Cd8+Rorc+Ptcra+Rag1+ thymic γδ T cells. SAP-dependent diversion of embryonic day 17 thymic γδ T cell clonotypes into the αβ T cell developmental pathway was associated with a decreased frequency of mature clonotypes in neonatal thymus, and an altered γδ TCR repertoire in the periphery. Finally, we identify TRGV4/TRAV13-4(DV7)-expressing T cells as a novel, SAP-dependent Vγ4 γδT1 subset. Together, the data support a model in which SAP-dependent γδ/αβ T cell lineage commitment regulates γδ T cell developmental programming and shapes the γδ TCR repertoire.

Keywords: T cells; gamma delta T cells; immunology; inflammation; mouse; thymic development.

MeSH terms

  • Animals
  • Cell Differentiation
  • Immunity, Innate
  • Intraepithelial Lymphocytes / immunology
  • Intraepithelial Lymphocytes / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Antigen, T-Cell, gamma-delta* / genetics
  • Receptors, Antigen, T-Cell, gamma-delta* / immunology
  • Receptors, Antigen, T-Cell, gamma-delta* / metabolism
  • Signal Transduction*
  • Signaling Lymphocytic Activation Molecule Associated Protein* / genetics
  • Signaling Lymphocytic Activation Molecule Associated Protein* / metabolism
  • Signaling Lymphocytic Activation Molecule Family
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Thymus Gland / immunology
  • Thymus Gland / metabolism

Substances

  • Receptors, Antigen, T-Cell, gamma-delta
  • Signaling Lymphocytic Activation Molecule Associated Protein
  • Sh2d1a protein, mouse
  • Slamf6 protein, mouse
  • Signaling Lymphocytic Activation Molecule Family

Associated data

  • GEO/GSE262064