Cell-Cycle-Dependent Reconfiguration of the DNA Methylome during Terminal Differentiation of Human B Cells into Plasma Cells

Cell Rep. 2015 Nov 3;13(5):1059-71. doi: 10.1016/j.celrep.2015.09.051. Epub 2015 Oct 22.

Abstract

Molecular mechanisms underlying terminal differentiation of B cells into plasma cells are major determinants of adaptive immunity but remain only partially understood. Here we present the transcriptional and epigenomic landscapes of cell subsets arising from activation of human naive B cells and differentiation into plasmablasts. Cell proliferation of activated B cells was linked to a slight decrease in DNA methylation levels, but followed by a committal step in which an S phase-synchronized differentiation switch was associated with an extensive DNA demethylation and local acquisition of 5-hydroxymethylcytosine at enhancers and genes related to plasma cell identity. Downregulation of both TGF-?1/SMAD3 signaling and p53 pathway supported this final step, allowing the emergence of a CD23-negative subpopulation in transition from B cells to plasma cells. Remarkably, hydroxymethylation of PRDM1, a gene essential for plasma cell fate, was coupled to progression in S phase, revealing an intricate connection among cell cycle, DNA (hydroxy)methylation, and cell fate determination.

Keywords: 5hmC; B cell differentiation; DNA methylation; plasma cell differentiation; plasmablast.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle*
  • Cells, Cultured
  • DNA Methylation*
  • Humans
  • Lymphopoiesis*
  • Plasma Cells / cytology*
  • Plasma Cells / metabolism
  • Positive Regulatory Domain I-Binding Factor 1
  • Receptors, IgE / genetics
  • Receptors, IgE / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Smad3 Protein / genetics
  • Smad3 Protein / metabolism
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Receptors, IgE
  • Repressor Proteins
  • SMAD3 protein, human
  • Smad3 Protein
  • Transforming Growth Factor beta
  • Tumor Suppressor Protein p53
  • PRDM1 protein, human
  • Positive Regulatory Domain I-Binding Factor 1