A20 intrinsically influences human effector T-cell survival and function by regulating both NF-κB and JNK signaling

Eur J Immunol. 2024 Dec;54(12):e2451245. doi: 10.1002/eji.202451245. Epub 2024 Oct 2.

Abstract

A20 is a dual-function ubiquitin-editing enzyme that maintains immune homeostasis by restraining inflammation. Although A20 serves a similar negative feedback function for T-cell receptor (TCR) signaling, the molecular mechanisms utilized and their ultimate impact on human T-cell function remain unclear. TCR engagement triggers the assembly of the CARD11-BCL10-MALT1 (CBM) protein complex, a signaling platform that governs the activation of downstream transcription factors including NF-κB and c-Jun/AP-1. Utilizing WT and A20 knockout Jurkat T cells, we found that A20 is required to negatively regulate NF-κB and JNK. Utilizing a novel set of A20 mutants in NF-κB and AP-1-driven reporter systems, we discovered the ZnF7 domain is crucial for negative regulatory capacity, while deubiquitinase activity is dispensable. Successful inactivation of A20 in human primary effector T cells congruently conferred sustained NF-κB and JNK signaling, including enhanced upregulation of activation markers, and increased secretion of several cytokines including IL-9. Finally, loss of A20 in primary human T cells resulted in decreased sensitivity to restimulation-induced cell death and increased sensitivity to cytokine withdrawal-induced death. These findings demonstrate the importance of A20 in maintaining T-cell homeostasis via negative regulation of both NF-κB and JNK signaling.

Keywords: Apoptosis; Cellular immunology; Cytokines; Signal transduction; T cells.

MeSH terms

  • Cell Survival* / immunology
  • Humans
  • Jurkat Cells
  • Lymphocyte Activation / immunology
  • MAP Kinase Signaling System / immunology
  • NF-kappa B* / metabolism
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction / immunology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Tumor Necrosis Factor alpha-Induced Protein 3* / genetics
  • Tumor Necrosis Factor alpha-Induced Protein 3* / metabolism

Substances

  • Tumor Necrosis Factor alpha-Induced Protein 3
  • NF-kappa B
  • TNFAIP3 protein, human
  • Receptors, Antigen, T-Cell