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ZEB2 Directs Senescent and Cytotoxic Terminal Differentiation of CD8⁺ T Cells in Atherosclerosis


Abstract

Senescent cytotoxic CD8⁺ T cells accumulate in atherosclerotic plaques and are associated with adverse cardiovascular outcomes, yet the transcriptional mechanisms underlying this pathogenic state remain poorly understood. Using single-cell transcriptomic profiling of human carotid atherosclerotic plaques, we identified a population of CD8⁺ TEMRA cells exhibiting a coordinated senescence and cytotoxic gene program that preferentially localise to plaque shoulder and luminal regions associated with inflammation and plaque vulnerability. Trajectory and gene-regulatory network analyses identified ZEB2 (zinc finger E-box binding homeobox 2), encoded within a coronary artery disease susceptibility locus, as a master regulator of this state. CRISPR-mediated deletion of ZEB2 in primary human CD8⁺ T cells impaired Granzyme B-mediated cytotoxicity and senescence. Accordingly, CD8⁺ T cell–specific or Granzyme B-restricted Zeb2 deletion in hypercholesterolaemic mice reduced atherosclerosis burden, macrophage accumulation, plaque necrosis, and inflammation. These findings establish ZEB2 as a transcriptional regulator that couples cytotoxic differentiation and senescence in CD8⁺ T cells and establishes this program as a driver of atherosclerosis progression.


Repository overview

This repository contains the R code used to generate all main and extended figures in the manuscript. Each script corresponds to one figure and is self-contained. Scripts are numbered to match figure numbers in the paper.

.
├── Figure_1_CD8_github.R   # scRNA-seq CD8 landscape, UCell module scoring, correlations
├── Figure_2_CD8_github.R   # CyTOF processing, RPCA integration, label transfer
├── Figure_3_CD8_github.R   # TEMRA module associations, MiloR differential abundance
├── Figure_4_CD8_github.R   # Slingshot pseudotime, tradeSeq GAM, ZEB2 Nebulosa
├── Figure_5_CD8_github.R   # ZEB2 DEG analysis, TF-module correlations, KO heatmap
├── Figure_7_CD8_github.R   # Mouse PBMC CyTOF (ZEB2 KO), CATALYST pipeline
└── README.md

Each script contains:

  • A header block listing input files, output files (by panel), and reporting standards
  • Section headers aligned to individual figure panels
  • Inline comments explaining analytical choices

Data availability

Dataset Description Accession
Human carotid scRNA-seq Gene Exprerssion Omnibus GSE224273, GSE235437, GSE246318
Human and Mouse CyTOF data ZENODO https://doi.org/10.5281/zenodo.20721348

System requirements

Software

Software Version tested Notes
R ≥ 4.3
Bioconductor ≥ 3.18

R packages

Single-cell RNA-seq (Figures 1–5)

Package Version tested Source
Seurat ≥ 5.0 CRAN
SeuratDisk ≥ 0.0.0.9021 GitHub (mojaveazure)
SeuratWrappers ≥ 0.3.5 GitHub (satijalab)
UCell ≥ 2.6 Bioconductor
slingshot ≥ 2.10 Bioconductor
tradeSeq ≥ 1.16 Bioconductor
TrajectoryUtils ≥ 1.10 Bioconductor
SingleCellExperiment ≥ 1.24 Bioconductor
miloR ≥ 2.0 Bioconductor
scater ≥ 1.30 Bioconductor
Nebulosa ≥ 1.12 Bioconductor

CyTOF (Figures 2 & 7)

Package Version tested Source
CATALYST ≥ 1.26 Bioconductor
flowCore ≥ 2.14 Bioconductor
Spectre ≥ 1.1.0 GitHub (ImmuneDynamics)

Visualisation and utilities

Package Version tested Source
ggplot2 ≥ 3.5 CRAN
patchwork ≥ 1.2 CRAN
cowplot ≥ 1.1 CRAN
ComplexHeatmap ≥ 2.18 Bioconductor
corrplot ≥ 0.92 CRAN
EnhancedVolcano ≥ 1.20 Bioconductor
fmsb ≥ 0.7 CRAN
ggalluvial ≥ 0.12 CRAN
pheatmap ≥ 1.0.12 CRAN
viridis ≥ 0.6 CRAN
RColorBrewer ≥ 1.1 CRAN
colorspace ≥ 2.1 CRAN
dplyr ≥ 1.1 CRAN
data.table ≥ 1.15 CRAN
tidyr ≥ 1.3 CRAN
readxl ≥ 1.4 CRAN
openxlsx ≥ 4.2 CRAN
matrixStats ≥ 1.3 CRAN
reticulate ≥ 1.36 CRAN
scCustomize ≥ 2.1 CRAN

Hardware

All analyses were run on a macOS system with ≥ 32 GB RAM.


Reproducibility

  • All scripts call set.seed(123) (or set.seed(1234) for Figure 7) at the top.
  • Random seeds for UMAP and FlowSOM are passed explicitly to each function call.
  • Package versions used for the final figures are listed above. Minor version differences may produce slightly different UMAP layouts but will not affect statistical conclusions.

License

This code is released under the MIT License — see LICENSE for details.


Contact

For questions about the code or data, please open a GitHub Issue

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R code for: ZEB2 Directs Senescent and Cytotoxic Terminal Differentiation of CD8+ T Cells in Atherosclerosis

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