Smarcd1 subunit of SWI/SNF chromatin-remodeling complexes collaborates with E2a to promote murine lymphoid specification

Dev Cell. 2024 Dec 2;59(23):3124-3140.e8. doi: 10.1016/j.devcel.2024.08.007. Epub 2024 Sep 3.

Abstract

Lymphocyte development from murine hematopoietic stem cells (HSCs) entails a loss of self-renewal capacity and a progressive restriction of developmental potential. Previous research from our laboratory suggests that specialized assemblies of ATP-dependent SWI/SNF chromatin-remodeling complexes play lineage-specific roles during murine hematopoiesis. Here, we demonstrate that the Smarcd1 subunit is essential for specification of lymphoid cell fate from multipotent progenitors. Acute deletion of Smarcd1 in murine adult hematopoiesis leads to lymphopenia, characterized by a near-complete absence of early lymphoid progenitors and mature B and T cells, while the myeloid and erythroid lineages remain unaffected. Mechanistically, we demonstrate that Smarcd1 is essential for the coordinated activation of a lymphoid gene signature in murine multipotent progenitors. This is achieved by interacting with the E2a transcription factor at proximal promoters and by regulating the activity of distal enhancers. Globally, these findings identify Smarcd1 as an essential chromatin remodeler that governs lymphoid cell fate.

Keywords: E2a/Tcf3; SWI/SNF complexes; Smarcd1/BAF60a; active enhancers; chromatin remodeling; lymphoid priming; lymphopenia.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors
  • Cell Differentiation / genetics
  • Cell Lineage / genetics
  • Chromatin Assembly and Disassembly*
  • Chromosomal Proteins, Non-Histone* / genetics
  • Chromosomal Proteins, Non-Histone* / metabolism
  • Hematopoiesis / genetics
  • Hematopoietic Stem Cells* / cytology
  • Hematopoietic Stem Cells* / metabolism
  • Lymphocytes / cytology
  • Lymphocytes / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Promoter Regions, Genetic / genetics
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • Chromosomal Proteins, Non-Histone
  • Smarcd1 protein, mouse
  • Tcf3 protein, mouse
  • SWI-SNF-B chromatin-remodeling complex
  • Basic Helix-Loop-Helix Transcription Factors