TREM-2 promotes Th1 responses by interacting with the CD3ζ-ZAP70 complex following Mycobacterium tuberculosis infection

J Clin Invest. 2021 Sep 1;131(17):e137407. doi: 10.1172/JCI137407.

Abstract

Triggering receptor expressed on myeloid cells 2 (TREM-2) is a modulator of pattern recognition receptors on innate immune cells that regulates the inflammatory response. However, the role of TREM-2 in in vivo models of infection and inflammation remains controversial. Here, we demonstrated that TREM-2 expression on CD4+ T cells was induced by Mycobacterium tuberculosis infection in both humans and mice and positively associated with T cell activation and an effector memory phenotype. Activation of TREM-2 in CD4+ T cells was dependent on interaction with the putative TREM-2 ligand expressed on DCs. Unlike the observation in myeloid cells that TREM-2 signals through DAP12, in CD4+ T cells, TREM-2 interacted with the CD3ζ-ZAP70 complex as well as with the IFN-γ receptor, leading to STAT1/-4 activation and T-bet transcription. In addition, an infection model using reconstituted Rag2-/- mice (with TREM-2-KO vs. WT cells or TREM-2+ vs. TREM-2-CD4+ T cells) or CD4+ T cell-specific TREM-2 conditional KO mice demonstrated that TREM-2 promoted a Th1-mediated host defense against M. tuberculosis infection. Taken together, these findings reveal a critical role of TREM-2 in evoking proinflammatory Th1 responses that may provide potential therapeutic targets for infectious and inflammatory diseases.

Keywords: Adaptive immunity; Inflammation; T cell receptor; Tuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • CD3 Complex / immunology*
  • Disease Models, Animal
  • Female
  • Humans
  • Immunity, Innate
  • Lymphocyte Activation
  • Male
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Models, Immunological
  • Mycobacterium tuberculosis / immunology
  • Receptors, Immunologic / deficiency
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / immunology*
  • Receptors, Pattern Recognition / immunology
  • STAT Transcription Factors / immunology
  • Th1 Cells / immunology*
  • Tuberculosis / immunology*
  • ZAP-70 Protein-Tyrosine Kinase / immunology*

Substances

  • CD3 Complex
  • CD3 antigen, zeta chain
  • Membrane Glycoproteins
  • Receptors, Immunologic
  • Receptors, Pattern Recognition
  • STAT Transcription Factors
  • TREM2 protein, human
  • Trem2 protein, mouse
  • ZAP-70 Protein-Tyrosine Kinase
  • ZAP70 protein, human