The aryl hydrocarbon receptor controls cell-fate decisions in B cells

J Exp Med. 2017 Jan;214(1):197-208. doi: 10.1084/jem.20160789. Epub 2016 Dec 23.

Abstract

Generation of cellular heterogeneity is an essential feature of the adaptive immune system. This is best exemplified during humoral immune response when an expanding B cell clone assumes multiple cell fates, including class-switched B cells, antibody-secreting plasma cells, and memory B cells. Although each cell type is essential for immunity, their generation must be exquisitely controlled because a class-switched B cell cannot revert back to the parent isotype, and a terminally differentiated plasma cell cannot contribute to the memory pool. In this study, we show that an environmental sensor, the aryl hydrocarbon receptor (AhR) is highly induced upon B cell activation and serves a critical role in regulating activation-induced cell fate outcomes. We find that AhR negatively regulates class-switch recombination ex vivo by altering activation-induced cytidine deaminase expression. We further demonstrate that AhR suppresses class switching in vivo after influenza virus infection and immunization with model antigens. In addition, by regulating Blimp-1 expression via Bach2, AhR represses differentiation of B cells into plasmablasts ex vivo and antibody-secreting plasma cells in vivo. These experiments suggest that AhR serves as a molecular rheostat in B cells to brake the effector response, possibly to facilitate optimal recall responses. Thus, AhR might represent a novel molecular target for manipulation of B cell responses during vaccination.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / physiology*
  • Cell Differentiation
  • Cytidine Deaminase / physiology
  • Female
  • Immunoglobulin Class Switching
  • Influenza A Virus, H1N1 Subtype / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Plasma Cells / cytology
  • Polychlorinated Dibenzodioxins / pharmacology
  • Positive Regulatory Domain I-Binding Factor 1
  • Receptors, Aryl Hydrocarbon / physiology*
  • T-Lymphocytes / physiology
  • Transcription Factors / physiology

Substances

  • Polychlorinated Dibenzodioxins
  • Prdm1 protein, mouse
  • Receptors, Aryl Hydrocarbon
  • Transcription Factors
  • Positive Regulatory Domain I-Binding Factor 1
  • AICDA (activation-induced cytidine deaminase)
  • Cytidine Deaminase