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

Yoshitaka Adachi, Seitaro Terakura, Masahide Osaki, Yusuke Okuno, Yoshitaka Sato, Ken Sagou, Yuki Takeuchi, Hirofumi Yokota, Kanae Imai, Peter Steinberger, Judith Leitner, Ryo Hanajiri, Makoto Murata, Hitoshi Kiyoi

2024Nature Communications18 citationsDOIOpen Access PDF

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. Chimeric antigen receptor (CAR) T cell therapy is a promising cancer treatment, but further optimization is still direly needed. Here the authors perform a CRISPR screen in CAR T cells to find Cul5 as a negative regulator, with Cul5 deficiency and subsequently enhanced JAK/STAT signaling attributed to improved CAR T efficacy in mouse tumor models.

Topics & Concepts

EffectorCell biologystatJAK-STAT signaling pathwaySignal transductionChimeric antigen receptorReceptorBiologyChemistryT cellImmunologyReceptor tyrosine kinaseImmune systemGeneticsSTAT3CAR-T cell therapy researchImmune Cell Function and Interaction
Cullin-5 deficiency promotes chimeric antigen receptor T cell effector functions potentially via the modulation of JAK/STAT signaling pathway | Litcius