The T-cell fingerprint of MALT1 paracaspase revealed by selective inhibition

Immunol Cell Biol. 2018 Jan;96(1):81-99. doi: 10.1111/imcb.1018. Epub 2017 Dec 21.

Abstract

Mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT1) is essential for immune responses triggered by antigen receptors but the contribution of its paracaspase activity is not fully understood. Here, we studied how MALT1 proteolytic function regulates T-cell activation and fate after engagement of the T-cell receptor pathway. We show that MLT-827, a potent and selective MALT1 paracaspase inhibitor, does not prevent the initial phase of T-cell activation, in contrast to the pan-protein kinase C inhibitor AEB071. However, MLT-827 strongly impacted cell expansion after activation. We demonstrate this is the consequence of profound inhibition of IL-2 production as well as reduced expression of the IL-2 receptor alpha subunit (CD25), resulting from defective canonical NF-κB activation and accelerated mRNA turnover mechanisms. Accordingly, MLT-827 revealed a unique transcriptional fingerprint of MALT1 protease activity, providing evidence for broad control of T-cell signaling pathways. Altogether, this first report with a potent and selective inhibitor elucidates how MALT1 paracaspase activity integrates several T-cell activation pathways and indirectly controls gamma-chain receptor dependent survival, to impact on T-cell expansion.

Keywords: Interleukin‐2; MALT1 paracaspase; NF‐kappaB; T‐cell receptor; T‐cell survival; protease inhibitor; signal transduction.

MeSH terms

  • Cell Proliferation
  • Cell Survival
  • Cells, Cultured
  • Gene Expression Regulation
  • Humans
  • Immunomodulation
  • Interleukin-2 / metabolism
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Lymphocyte Activation
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / metabolism*
  • NF-kappa B / metabolism*
  • Proteolysis
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction
  • T-Lymphocytes / immunology*

Substances

  • Interleukin-2
  • Interleukin-2 Receptor alpha Subunit
  • NF-kappa B
  • Receptors, Antigen, T-Cell
  • MALT1 protein, human
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein