YY1 knockout in pro-B cells impairs lineage commitment, enabling unusual hematopoietic lineage plasticity

Genes Dev. 2024 Oct 16;38(17-20):887-914. doi: 10.1101/gad.351734.124.

Abstract

During B-cell development, cells progress through multiple developmental stages, with the pro-B-cell stage defining commitment to the B-cell lineage. YY1 is a ubiquitous transcription factor that is capable of both activation and repression functions. We found here that knockout of YY1 at the pro-B-cell stage eliminates B lineage commitment. YY1 knockout pro-B cells can generate T lineage cells in vitro using the OP9-DL4 feeder system and in vivo after injection into sublethally irradiated Rag1-/- mice. These T lineage-like cells lose their B lineage transcript profile and gain a T-cell lineage profile. Single-cell RNA-seq experiments showed that as YY1 knockout pro-B cells transition into T lineage cells in vitro, various cell clusters adopt transcript profiles representing a multiplicity of hematopoietic lineages, indicating unusual lineage plasticity. In addition, YY1 KO pro-B cells in vivo can give rise to other hematopoietic lineages in vivo. Evaluation of RNA-seq, scRNA-seq, ChIP-seq, and scATAC-seq data indicates that YY1 controls numerous chromatin-modifying proteins leading to increased accessibility of alternative lineage genes in YY1 knockout pro-B cells. Given the ubiquitous nature of YY1 and its dual activation and repression functions, YY1 may regulate commitment in multiple cell lineages.

Keywords: B-cell development; YY1; alternative lineages; hematopoietic lineage plasticity; lineage commitment; scATAC-seq; scRNA-seq; transcription.

MeSH terms

  • Animals
  • B-Lymphocytes / cytology
  • B-Lymphocytes / metabolism
  • Cell Differentiation / genetics
  • Cell Lineage* / genetics
  • Gene Knockout Techniques
  • Hematopoiesis / genetics
  • Mice
  • Mice, Knockout
  • Precursor Cells, B-Lymphoid* / cytology
  • Precursor Cells, B-Lymphoid* / metabolism
  • T-Lymphocytes / cytology
  • YY1 Transcription Factor* / genetics
  • YY1 Transcription Factor* / metabolism

Substances

  • Yy1 protein, mouse
  • YY1 Transcription Factor