Base-editing mutagenesis maps alleles to tune human T cell functions

Nature. 2024 Jan;625(7996):805-812. doi: 10.1038/s41586-023-06835-6. Epub 2023 Dec 13.

Abstract

CRISPR-enabled screening is a powerful tool for the discovery of genes that control T cell function and has nominated candidate targets for immunotherapies1-6. However, new approaches are required to probe specific nucleotide sequences within key genes. Systematic mutagenesis in primary human T cells could reveal alleles that tune specific phenotypes. DNA base editors are powerful tools for introducing targeted mutations with high efficiency7,8. Here we develop a large-scale base-editing mutagenesis platform with the goal of pinpointing nucleotides that encode amino acid residues that tune primary human T cell activation responses. We generated a library of around 117,000 single guide RNA molecules targeting base editors to protein-coding sites across 385 genes implicated in T cell function and systematically identified protein domains and specific amino acid residues that regulate T cell activation and cytokine production. We found a broad spectrum of alleles with variants encoding critical residues in proteins including PIK3CD, VAV1, LCP2, PLCG1 and DGKZ, including both gain-of-function and loss-of-function mutations. We validated the functional effects of many alleles and further demonstrated that base-editing hits could positively and negatively tune T cell cytotoxic function. Finally, higher-resolution screening using a base editor with relaxed protospacer-adjacent motif requirements9 (NG versus NGG) revealed specific structural domains and protein-protein interaction sites that can be targeted to tune T cell functions. Base-editing screens in primary immune cells thus provide biochemical insights with the potential to accelerate immunotherapy design.

MeSH terms

  • Alleles*
  • Amino Acids / genetics
  • CRISPR-Cas Systems / genetics
  • Cytokines / biosynthesis
  • Cytokines / metabolism
  • Gain of Function Mutation
  • Gene Editing*
  • Humans
  • Loss of Function Mutation
  • Lymphocyte Activation
  • Mutagenesis* / genetics
  • RNA, Guide, CRISPR-Cas Systems / genetics
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism

Substances

  • Amino Acids
  • RNA, Guide, CRISPR-Cas Systems
  • PIK3CD protein, human
  • VAV1 protein, human
  • SLP-76 signal Transducing adaptor proteins
  • PLCG2 protein, human
  • Cytokines