Indirect suppression of CD4 T cell activation through LAG-3-mediated trans-endocytosis of MHC class II

Cell Rep. 2024 Sep 24;43(9):114655. doi: 10.1016/j.celrep.2024.114655. Epub 2024 Aug 26.

Abstract

Blockade of immune checkpoint receptors has shown outstanding efficacy for tumor immunotherapy. Promising treatment with anti-lymphocyte-activation gene-3 (LAG-3) has already been recognized as the next efficacious treatment, but there is still limited understanding of the mechanism of LAG-3-mediated immune suppression. Here, utilizing high-resolution molecular imaging, we find a mechanism of CD4 T cell suppression via LAG-3, in which LAG-3-bound major histocompatibility complex (MHC) class II molecules on antigen-presenting cells (APCs) gather at the central region of an immunological synapse and are trans-endocytosed by T cell receptor-driven internalization motility toward CD4 and CD8 T cells expressing LAG-3. Downregulation of MHC class II molecules on APCs thus results in the attenuation of their antigen-presentation function and impairment of CD4 T cell activation. From these data, anti-LAG-3 treatment is suggested to have potency to directly block the inhibitory signaling via LAG-3 and simultaneously reduce MHC class II expression on APCs by LAG-3-mediated trans-endocytosis for recovery from T cell exhaustion.

Keywords: CP: Immunology; LAG-3; MHC class II; T cell; T cell receptor internalization; indirect suppression; trans-endocytosis.

MeSH terms

  • Animals
  • Antigen Presentation / immunology
  • Antigen-Presenting Cells / immunology
  • Antigen-Presenting Cells / metabolism
  • Antigens, CD* / metabolism
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Endocytosis
  • Histocompatibility Antigens Class II* / immunology
  • Histocompatibility Antigens Class II* / metabolism
  • Humans
  • Lymphocyte Activation Gene 3 Protein*
  • Lymphocyte Activation* / immunology
  • Mice
  • Mice, Inbred C57BL

Substances

  • Lymphocyte Activation Gene 3 Protein
  • Histocompatibility Antigens Class II
  • Antigens, CD
  • Lag3 protein, mouse