Cullin-5 deficiency promotes chimeric antigen receptor T cell effector functions potentially via the modulation of JAK/STAT signaling pathway

Nat Commun. 2024 Dec 10;15(1):10376. doi: 10.1038/s41467-024-54794-x.

Abstract

Chimeric antigen receptor (CAR) T cell is a promising therapy for cancer, but factors that enhance the efficacy of CAR T cell remain elusive. Here we perform a genome-wide CRISPR screening to probe genes that regulate the proliferation and survival of CAR T cells following repetitive antigen stimulations. We find that genetic ablation of CUL5, encoding a core element of the multi-protein E3 ubiquitin-protein ligase complex, cullin-RING ligase 5, enhances human CD19 CAR T cell expansion potential and effector functions, potentially via the Janus kinase/signal transducers and activators of transcription (JAK/STAT) pathway. In this regard, CUL5 knockout CD19 CAR T cells show sustained STAT3 and STAT5 phosphorylation, as well as delayed phosphorylation and degradation of JAK1 and JAK3. In vivo, shRNA-mediated knockdown of CUL5 enhances CD19 CAR T treatment outcomes in tumor-bearing mice. Our findings thus imply that targeting CUL5 in the ubiquitin system may enhance CAR T cell effector functions to enhance immunotherapy efficacy.

MeSH terms

  • Animals
  • Antigens, CD19 / immunology
  • Antigens, CD19 / metabolism
  • CRISPR-Cas Systems
  • Cell Line, Tumor
  • Cell Proliferation
  • Cullin Proteins* / genetics
  • Cullin Proteins* / metabolism
  • Humans
  • Immunotherapy, Adoptive / methods
  • Janus Kinases / metabolism
  • Mice
  • Phosphorylation
  • Receptors, Chimeric Antigen* / immunology
  • Receptors, Chimeric Antigen* / metabolism
  • STAT Transcription Factors / metabolism
  • STAT3 Transcription Factor / metabolism
  • STAT5 Transcription Factor / genetics
  • STAT5 Transcription Factor / metabolism
  • Signal Transduction*
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Cullin Proteins
  • Receptors, Chimeric Antigen
  • CUL5 protein, human
  • Antigens, CD19
  • STAT3 Transcription Factor
  • Janus Kinases
  • STAT5 Transcription Factor
  • STAT Transcription Factors