Progression from the Common Lymphoid Progenitor to B/Myeloid PreproB and ProB Precursors during B Lymphopoiesis Requires C/EBPα

J Immunol. 2018 Sep 15;201(6):1692-1704. doi: 10.4049/jimmunol.1800244. Epub 2018 Jul 30.

Abstract

The C/EBPα transcription factor is required for myelopoiesis, with prior observations suggesting additional contributions to B lymphopoiesis. Cebpa expression is evident in common lymphoid progenitor (CLP) and preproB cells but is absent in proB and preB cells. We previously observed that marrow lacking the Cebpa +37 kb enhancer is impaired in producing B cells upon competitive transplantation. Additionally, a Cebpa enhancer/promoter-hCD4 transgene is expressed in B/myeloid CFU. Extending these findings, pan-hematopoietic murine Cebpa enhancer deletion using Mx1-Cre leads to expanded CLP, fewer preproB cells, markedly reduced proB and preB cells, and reduced mature B cells, without affecting T cell numbers. In contrast, enhancer deletion at the proB stage using Mb1-Cre does not impair B cell maturation. Further evaluation of CLP reveals that the Cebpa transgene is expressed almost exclusively in Flt3+ multipotent CLP versus B cell-restricted Flt3- CLP. In vitro, hCD4+ preproB cells produce both B and myeloid cells, whereas hCD4- preproB cells only produce B cells. Additionally, a subset of hCD4- preproB cells express high levels of RAG1-GFP, as seen also in proB cells. Global gene expression analysis indicates that hCD4+ preproB cells express proliferative pathways, whereas B cell development and signal transduction pathways predominate in hCD4- preproB cells. Consistent with these changes, Cebpa enhancer-deleted preproB cells downmodulate cell cycle pathways while upregulating B cell signaling pathways. Collectively, these findings indicate that C/EBPα is required for Flt3+ CLP maturation into preproB cells and then for proliferative Cebpaint B/myeloid preproB cells to progress to Cebpalo B cell-restricted preproB cells and finally to Cebpaneg proB cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CCAAT-Enhancer-Binding Proteins / genetics
  • CCAAT-Enhancer-Binding Proteins / immunology*
  • CD4 Antigens / genetics
  • CD4 Antigens / immunology
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology*
  • Humans
  • Lymphopoiesis / genetics
  • Lymphopoiesis / immunology*
  • Mice
  • Mice, Transgenic
  • Myeloid Progenitor Cells / cytology
  • Myeloid Progenitor Cells / immunology*
  • Precursor Cells, B-Lymphoid / cytology
  • Precursor Cells, B-Lymphoid / immunology*

Substances

  • CCAAT-Enhancer-Binding Proteins
  • CD4 Antigens
  • CEBPA protein, mouse