Pathogenic TH17 inflammation is sustained in the lungs by conventional dendritic cells and Toll-like receptor 4 signaling

J Allergy Clin Immunol. 2018 Oct;142(4):1229-1242.e6. doi: 10.1016/j.jaci.2017.10.023. Epub 2017 Nov 14.

Abstract

Background: Mechanisms that elicit mucosal TH17 cell responses have been described, yet how these cells are sustained in chronically inflamed tissues remains unclear.

Objective: We sought to understand whether maintenance of lung TH17 inflammation requires environmental agents in addition to antigen and to identify the lung antigen-presenting cell (APC) types that sustain the self-renewal of TH17 cells.

Methods: Animals were exposed repeatedly to aspiration of ovalbumin alone or together with environmental adjuvants, including common house dust extract (HDE), to test their role in maintaining lung inflammation. Alternatively, antigen-specific effector/memory TH17 cells, generated in culture with CD4+ T cells from Il17a fate-mapping mice, were adoptively transferred to assess their persistence in genetically modified animals lacking distinct lung APC subsets or cell-specific Toll-like receptor (TLR) 4 signaling. TH17 cells were also cocultured with lung APC subsets to determine which of these could revive their expansion and activation.

Results: TH17 cells and the consequent neutrophilic inflammation were poorly sustained by inhaled antigen alone but were augmented by inhalation of antigen together with HDE. This was associated with weight loss and changes in lung physiology consistent with interstitial lung disease. The effect of HDE required TLR4 signaling predominantly in lung hematopoietic cells, including CD11c+ cells. CD103+ and CD11b+ conventional dendritic cells interacted directly with TH17 cells in situ and revived the clonal expansion of TH17 cells both ex vivo and in vivo, whereas lung macrophages and B cells could not.

Conclusion: TH17-dependent inflammation in the lungs can be sustained by persistent TLR4-mediated activation of lung conventional dendritic cells.

Keywords: T(H)17 cells; Toll-like receptor 4; chronic inflammation; dendritic cells; house dust extract.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Allergens / immunology
  • Animals
  • Aspergillus oryzae / immunology
  • Dendritic Cells / immunology*
  • Dust
  • Endotoxins / immunology
  • Inflammation / immunology*
  • Lung / immunology*
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Ovalbumin / immunology
  • Th17 Cells / immunology*
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology*

Substances

  • Allergens
  • Dust
  • Endotoxins
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Ovalbumin