Blimp-1 is essential for allergen-induced asthma and Th2 cell development in the lung

J Exp Med. 2020 Jul 6;217(7):e20190742. doi: 10.1084/jem.20190742.

Abstract

A Th2 immune response is central to allergic airway inflammation, which afflicts millions worldwide. However, the mechanisms that augment GATA3 expression in an antigen-primed developing Th2 cell are not well understood. Here, we describe an unexpected role for Blimp-1, a transcriptional repressor that constrains autoimmunity, as an upstream promoter of GATA3 expression that is critical for Th2 cell development in the lung to inhaled but not systemically delivered allergens but is dispensable for TFH function and IgE production. Mechanistically, Blimp-1 acts through Bcl6, leading to increased GATA3 expression in lung Th2 cells. Surprisingly, the anti-inflammatory cytokine IL-10, but not the pro-inflammatory cytokines IL-6 or IL-21, is required via STAT3 activation to up-regulate Blimp-1 and promote Th2 cell development. These data reveal a hitherto unappreciated role for an IL-10-STAT3-Blimp-1 circuit as an initiator of an inflammatory Th2 response in the lung to allergens. Thus, Blimp-1 in a context-dependent fashion can drive inflammation by promoting rather than terminating effector T cell responses.

Publication types

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

MeSH terms

  • Allergens / immunology*
  • Animals
  • Asthma / complications
  • Asthma / immunology*
  • Cell Differentiation
  • GATA3 Transcription Factor / metabolism
  • Immunoglobulin E / metabolism
  • Inflammation / pathology
  • Interleukin-6 / metabolism
  • Interleukins / metabolism
  • Lung / immunology*
  • Lung / pathology*
  • Lymph Nodes / metabolism
  • Mice, Inbred C57BL
  • Organ Specificity
  • Positive Regulatory Domain I-Binding Factor 1 / metabolism*
  • Proto-Oncogene Proteins c-bcl-6 / metabolism
  • Pyroglyphidae / immunology
  • Receptors, Interleukin-21 / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • T-Lymphocytes, Helper-Inducer / metabolism
  • Th2 Cells / immunology*

Substances

  • Allergens
  • Bcl6 protein, mouse
  • GATA3 Transcription Factor
  • Interleukin-6
  • Interleukins
  • Proto-Oncogene Proteins c-bcl-6
  • Receptors, Interleukin-21
  • STAT3 Transcription Factor
  • Immunoglobulin E
  • Positive Regulatory Domain I-Binding Factor 1
  • interleukin-21