Peipei Wang, Jieying Li, Wei Wang, Zhuoyue Meng, Huixin Wu, Shumin Du, Kai Deng, Jinfeng Cai
Together, our findings uncover an unexpected role of Vpr in inducing lineage-associated transcriptional reprogramming in mature CD4+ T cells and provide new insight into how HIV-1 manipulates host-cell identity during infection.
CD4+ T cells are the principal cellular targets of HIV-1, yet the extent to which viral proteins reshape their transcriptional identity remains incompletely understood. Here, using an integrated multi-omics approach, we identified a distinct population of HIV-1 RNA-positive CD4+ T cells that localized within transcriptionally defined B-cell clusters and expressed multiple canonical B cell-associated genes during acute infection. Mechanistic analyses revealed that this phenotype was driven by the HIV-1 accessory protein Vpr. Both Vpr overexpression and Vpr-deficient viral systems demonstrated that Vpr induces the expression of CD19, MS4A1, CD22, and PAX5 in primary CD4+ T cells. Single-cell RNA sequencing, bulk RNA sequencing, and assay for transposase-accessible chromatin using sequencing (ATAC-seq) further showed that Vpr promotes extensive transcriptional and epigenetic remodeling, accompanied by increased accessibility and expression of genes involved in B-cell differentiation and development, including PAX5, EBF1, and PRDM1. Notably, this B cell-like transcriptional program was transient and gradually diminished during prolonged culture. Together, our findings uncover an unexpected role of Vpr in inducing lineage-associated transcriptional reprogramming in mature CD4+ T cells and provide new insight into how HIV-1 manipulates host-cell identity during infection.