Transcription factors GATA-3 and RORγt are important for determining the phenotype of allergic airway inflammation in a murine model of asthma

J Immunol. 2013 Feb 1;190(3):1056-65. doi: 10.4049/jimmunol.1202386. Epub 2013 Jan 4.

Abstract

In refractory asthma, neutrophils, rather than eosinophils, often predominate in the airways. Neutrophilic airway inflammation appears to be resistant to steroids and may be related to the Th17, rather than the Th2, cytokine milieu. However, the role of GATA-3 and RORγt, transcription factors for Th2 and Th17 cell differentiation, respectively, in the pathogenesis of steroid-insensitive asthma remains unclear. To examine the effect of GATA-3- and RORγt-overexpression backgrounds on airway inflammation and steroid sensitivity, we generated two strains of transgenic mice overexpressing GATA-3 or RORγt. Mice were sensitized and challenged with OVA. Some OVA-sensitized/challenged mice were treated with dexamethasone, anti-IL-17 Ab, CXCR2 antagonist, or anti-IL-6R Ab to demonstrate their therapeutic effects on airway inflammation. Although Ag-specific airway inflammation and hyperresponsiveness were induced in each mouse, the phenotype of inflammation showed a distinct difference that was dependent upon the genotype. GATA-3-overexpressing mice exhibited steroid-sensitive eosinophilic inflammation with goblet cell hyperplasia and mucus hyperproduction under Th2-biased conditions, and RORγt-overexpressing mice developed steroid-insensitive neutrophilic inflammation under Th17-biased conditions. The levels of keratinocyte-derived chemokine, MIP-2, IL-6, and other neutrophil chemotaxis-related mediators were significantly elevated in OVA-exposed RORγt-overexpressing mice compared with wild-type mice. Interestingly, airway hyperresponsiveness accompanied by neutrophilic airway inflammation in RORγt-overexpressing mice was effectively suppressed by anti-IL-17 Ab, CXCR2 antagonist, or anti-IL-6R Ab administration. In conclusion, our results suggest that the expression levels of GATA-3 and RORγt may be important for determining the phenotype of asthmatic airway inflammation. Furthermore, blockade of the Th17-signaling pathway may be a treatment option for steroid-insensitive asthma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asthma / genetics*
  • Asthma / immunology
  • Chemokines / biosynthesis
  • Chemokines / genetics
  • Disease Models, Animal
  • Female
  • GATA3 Transcription Factor / biosynthesis
  • GATA3 Transcription Factor / genetics
  • GATA3 Transcription Factor / physiology*
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / immunology
  • Immunoglobulin E / blood
  • Immunoglobulin E / immunology
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / physiology
  • Lung / immunology
  • Lung / pathology
  • Lymphokines / biosynthesis
  • Lymphokines / genetics
  • Lymphopoiesis / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neutrophils / immunology
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / biosynthesis
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / genetics
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / physiology*
  • Ovalbumin / immunology
  • Ovalbumin / toxicity
  • Phenotype
  • Receptors, Interleukin-6 / antagonists & inhibitors
  • Receptors, Interleukin-8B / antagonists & inhibitors
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / physiology
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Th2 Cells / immunology*
  • Th2 Cells / metabolism

Substances

  • Chemokines
  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • Interleukin-17
  • Lymphokines
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Receptors, Interleukin-6
  • Receptors, Interleukin-8B
  • Recombinant Fusion Proteins
  • Rorc protein, mouse
  • Immunoglobulin E
  • Ovalbumin