Lung dendritic cells induce T(H)17 cells that produce T(H)2 cytokines, express GATA-3, and promote airway inflammation

J Allergy Clin Immunol. 2011 Jul;128(1):192-201.e6. doi: 10.1016/j.jaci.2011.04.029. Epub 2011 May 20.

Abstract

Background: Dendritic cells (DCs) are crucial to shape the adaptive immune response. Extensive in vitro manipulation reprograms T(H)2 and T(H)17 cell lines into T(H)1 cells, leading to the concept of CD4(+) T(H) cell subset plasticity. The conversion of memory T(H)17 cells into T(H)2 cells or vice versa remains to be clarified.

Objective: We examined the localization of T(H)17/T(H)2 cells in vivo, their cellular origin (T(H)2 vs T(H)17), and the underlying mechanisms that drive the generation of these double T(H) producers.

Methods: Antigen-loaded bone marrow-derived DCs (ovalbumin-DCs) were repeatedly administered locally (intratracheally) or systemically (intravenously) to naive mice to elicit chronic airway inflammation. Inflamed lungs and mediastinal lymph nodes were examined for the presence of IL-17(+)IL-13(+)IL-4(+)CD4(+) T cells that coexpressed retinoic acid receptor-related orphan receptor γt and GATA-3 (T(H)17/T(H)2).

Results: We show that repetitive administration of inflammatory ovalbumin-DCs, locally or systemically, promoted the development of antigen-specific T(H)17/T(H)2 cells in lungs and mediastinal lymph nodes. Immunized mice had IgE-independent and steroid-resistant airway inflammation with a mixed neutrophil and eosinophil infiltration of the bronchoalveolar lavage fluid. Airway inflammatory signal regulatory protein α-positive DCs reprogrammed in vitro-generated T(H)17 but not T(H)2 cells, as well as lung effector T(H) cells, into T(H)17/T(H)2 cells.

Conclusion: We demonstrate the existence of T(H)17/T(H)2 cells that express GATA-3 in inflamed tissues and their T(H)17 origin. We further propose that repeated immunization with inflammatory DCs prevails on the route of DC administration to drive T(H)17/T(H)2-associated chronic lung inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / immunology
  • Cell Lineage
  • Cell Separation
  • Coculture Techniques
  • Cytokines / biosynthesis
  • Cytokines / immunology
  • Dendritic Cells / immunology*
  • Female
  • Flow Cytometry
  • GATA3 Transcription Factor / biosynthesis*
  • GATA3 Transcription Factor / immunology
  • Lung / cytology
  • Lung / immunology*
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred BALB C
  • Pneumonia / immunology*
  • Pneumonia / metabolism
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • Th17 Cells / cytology
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Th2 Cells / cytology
  • Th2 Cells / immunology
  • Th2 Cells / metabolism

Substances

  • Cytokines
  • GATA3 Transcription Factor
  • Gata3 protein, mouse