Pneumocystis-Driven Inducible Bronchus-Associated Lymphoid Tissue Formation Requires Th2 and Th17 Immunity

Cell Rep. 2017 Mar 28;18(13):3078-3090. doi: 10.1016/j.celrep.2017.03.016.

Abstract

Inducible bronchus-associated lymphoid tissue (iBALT) is an ectopic lymphoid structure composed of highly organized T cell and B cell zones that forms in the lung in response to infectious or inflammatory stimuli. Here, we develop a model for fungal-mediated iBALT formation, using infection with Pneumocystis that induces development of pulmonary lymphoid follicles. Pneumocystis-dependent iBALT structure formation and organization required CXCL13 signaling. Cxcl13 expression was regulated by interleukin (IL)-17 family members, as Il17ra-/-, Il17rb-/-, and Il17rc-/- mice failed to develop iBALT. Interestingly, Il17rb-/- mice have intact Th17 responses, but failed to generate an anti-Pneumocystis Th2 response. Given a role for Th2 and Th17 immunity in iBALT formation, we demonstrated that primary pulmonary fibroblasts synergistically upregulated Cxcl13 transcription following dual stimulation with IL-13 and IL-17A in a STAT3/GATA3-dependent manner. Together, these findings uncover a role for Th2/Th17 cells in regulating Cxcl13 expression and provide an experimental model for fungal-driven iBALT formation.

Keywords: Cxcl13; Pneumocystis; Th17; Th2; fungus; iBALT; immunity; lymphoid tissue.

MeSH terms

  • Animals
  • Bronchi / pathology*
  • Chemokine CXCL13 / metabolism
  • GATA3 Transcription Factor / metabolism
  • Immunity*
  • Interleukin-13 / metabolism
  • Interleukin-17 / metabolism
  • Lymphoid Tissue / pathology*
  • Lymphotoxin-alpha / metabolism
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Pneumocystis / physiology*
  • Pneumocystis Infections / immunology*
  • Pneumocystis Infections / microbiology
  • Pneumocystis Infections / prevention & control
  • Receptors, CXCR5 / metabolism
  • Receptors, Interleukin-17 / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Th17 Cells / immunology*
  • Th2 Cells / immunology*

Substances

  • CXCR5 protein, mouse
  • Chemokine CXCL13
  • GATA3 Transcription Factor
  • Interleukin-13
  • Interleukin-17
  • Lymphotoxin-alpha
  • Receptors, CXCR5
  • Receptors, Interleukin-17
  • STAT3 Transcription Factor