AMBRA1 controls the translation of immune-specific genes in T lymphocytes

Proc Natl Acad Sci U S A. 2024 Oct 29;121(44):e2416722121. doi: 10.1073/pnas.2416722121. Epub 2024 Oct 22.

Abstract

T cell receptor (TCR) engagement causes a global cellular response that entrains signaling pathways, cell cycle regulation, and cell death. The molecular regulation of mRNA translation in these processes is poorly understood. Using a whole-genome CRISPR screen for regulators of CD95 (FAS/APO-1)-mediated T cell death, we identified AMBRA1, a protein previously studied for its roles in autophagy, E3 ubiquitin ligase activity, and cyclin regulation. T cells lacking AMBRA1 resisted FAS-mediated cell death by down-regulating FAS expression at the translational level. We show that AMBRA1 is a vital regulator of ribosome protein biosynthesis and ribosome loading on select mRNAs, whereby it plays a key role in balancing TCR signaling with cell cycle regulation pathways. We also found that AMBRA1 itself is translationally controlled by TCR stimulation via the CD28-PI3K-mTORC1-EIF4F pathway. Together, these findings shed light on the molecular control of translation after T cell activation and implicate AMBRA1 as a translational regulator governing TCR signaling, cell cycle progression, and T cell death.

Keywords: AMBRA1; FAS signaling pathway; T cell activation; T cell death; protein translation.

MeSH terms

  • Adaptor Proteins, Signal Transducing* / genetics
  • Adaptor Proteins, Signal Transducing* / metabolism
  • Animals
  • CD28 Antigens / genetics
  • CD28 Antigens / metabolism
  • Gene Expression Regulation
  • Humans
  • Lymphocyte Activation
  • Mechanistic Target of Rapamycin Complex 1 / genetics
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Mice
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Biosynthesis
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction*
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism
  • fas Receptor / genetics
  • fas Receptor / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • CD28 Antigens
  • fas Receptor
  • Mechanistic Target of Rapamycin Complex 1
  • Phosphatidylinositol 3-Kinases
  • Receptors, Antigen, T-Cell
  • AMBRA1 protein, human