Dendritic cells conditioned by activin A-induced regulatory T cells exhibit enhanced tolerogenic properties and protect against experimental asthma

J Allergy Clin Immunol. 2018 Feb;141(2):671-684.e7. doi: 10.1016/j.jaci.2017.03.047. Epub 2017 Jun 1.

Abstract

Background: Previously, we demonstrated that regulatory T (Treg) cells induced by the cytokine activin-A suppress TH2-mediated allergic responses and linked airway disease. Still, the effects of activin-A-induced regulatory T (Act-A-iTreg) cells on the regulation of dendritic cell (DC)-driven allergic inflammation remain elusive.

Objective: Here we investigated whether Act-A-iTreg cells can modulate DC responses and endow them with enhanced tolerogenic functions.

Methods: Using adoptive cell transfer studies in mouse models of allergic airway disease, we examined the effects of Act-A-iTreg cells on DC phenotype, maturation status, and TH2 cell priming potential. Genome-wide gene expression profiling characterized the transcriptional networks induced in tolerogenic DCs by Act-A-iTreg cells. The ability of DCs conditioned by Act-A-iTreg cells (Act-A-iTreg cell-modified DCs) to protect against experimental asthma, and the mechanisms involved were also explored.

Results: Act-A-iTreg cell-modified DCs exhibited a significantly impaired capacity to uptake allergen and stimulate naive and TH2 effector responses on allergen stimulation in vivo accompanied by markedly attenuated inflammatory cytokine release in response to LPS. Gene-profiling studies revealed that Act-A-iTreg cells dampened crucial TH2-skewing transcriptional networks in DCs. Administration of Act-A-iTreg cell-modified DCs ameliorated cardinal asthma manifestations in preventive and therapeutic protocols through generation of strongly suppressive forkhead box P3+ Treg cells. Finally, programed death protein 1/programmed death ligand 1 signaling pathways were essential in potentiating the generation of DCs with tolerogenic properties by Act-A-iTreg cells.

Conclusion: Our studies reveal that Act-A-iTreg cells instruct the generation of a highly effective immunoregulatory circuit encompassing tolerogenic DCs and forkhead box P3+ Treg cells that could be targeted for the design of novel immunotherapies for allergic disorders.

Keywords: Activin-A; allergic asthma; immune regulation; regulatory T cells; tolerogenic dendritic cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activins / genetics
  • Activins / immunology*
  • Animals
  • Asthma / genetics
  • Asthma / immunology
  • Asthma / pathology
  • Asthma / prevention & control*
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / immunology
  • Dendritic Cells / immunology*
  • Dendritic Cells / pathology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / immunology
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • T-Lymphocytes, Regulatory
  • Th2 Cells / immunology
  • Th2 Cells / pathology
  • Transcription, Genetic / genetics
  • Transcription, Genetic / immunology

Substances

  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • activin A
  • Activins