Malt1 self-cleavage is critical for regulatory T cell homeostasis and anti-tumor immunity in mice

Eur J Immunol. 2018 Oct;48(10):1728-1738. doi: 10.1002/eji.201847597. Epub 2018 Aug 7.

Abstract

Mucosa-associated lymphoid tissue 1 (Malt1) regulates immune cell function by mediating the activation of nuclear factor κB (NF-κB) signaling through both its adaptor and proteolytic function. Malt1 is also a target of its own protease activity and this self-cleavage further contributes to NF-κB activity. Until now, the functional distinction between Malt1 self-cleavage and its general protease function in regulating NF-κB signaling and immune activation remained unclear. Here we demonstrate, using a new mouse model, the importance of Malt1 self-cleavage in regulating expression of NF-κB target genes and subsequent T cell activation. Significantly, we further establish that Treg homeostasis is critically linked to Malt1 function via a Treg intrinsic and extrinsic mechanism. TCR-mediated Malt1 proteolytic activity and self-cleavage was found to drive Il2 expression in conventional CD4+ T cells, thereby regulating Il2 availability for Treg homeostasis. Remarkably, the loss of Malt1-mediated self-cleavage alone was sufficient to cause a significant Treg deficit resulting in increased anti-tumor immune reactivity without associated autoimmunity complications. These results establish for the first time that inhibition of MALT1 proteolytic activity could be a viable therapeutic strategy to augment anti-tumor immunity.

Keywords: MALT1; NF-κB; Regulatory T cells; TCR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Gene Expression Regulation
  • Homeostasis
  • Interleukin-2 / immunology
  • Lymphocyte Activation*
  • Mice
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / genetics
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / immunology*
  • NF-kappa B / genetics
  • Neoplasm Proteins / immunology
  • Neoplasms / immunology*
  • Proteolysis
  • Signal Transduction / immunology
  • T-Lymphocytes, Regulatory / immunology*

Substances

  • Interleukin-2
  • NF-kappa B
  • Neoplasm Proteins
  • Malt1 protein, mouse
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein