STAT6 Signaling Attenuates Interleukin-17-Producing γδ T Cells during Acute Klebsiella pneumoniae Infection

Infect Immun. 2016 Apr 22;84(5):1548-1555. doi: 10.1128/IAI.00646-15. Print 2016 May.

Abstract

γδ T cells are prevalent at mucosal and epithelial surfaces and are a critical first line of defense against bacterial and fungal pathogens. γδ17 cells are a subset of γδ T cells which, in the presence of IL-23 and IL-1β, produce large quantities of interleukin-17A (IL-17A), a cytokine crucial to these cells' antibacterial and antifungal function. STAT6, an important transcription factor in Th2 differentiation and inhibition of Th1 differentiation, is expressed at high levels in the T cells of people with parasitic infections and asthma. Our group and others have shown that STAT6 attenuates IL-17A protein expression by CD4(+) T cells. By extension, we hypothesized that STAT6 activation also inhibits innate γδ17 cell cytokine secretion. We show here that γδ17 cells expressed the type I IL-4 receptor (IL-4R), and IL-4 increased STAT6 phosphorylation in γδ T cells. IL-4 inhibited γδ17 cell production of IL-17A. IL-4 also decreased γδ17 cell expression of IL-23R as well as Sgk1. To determine whether STAT6 signaling regulates γδ17 cell numbers in vivo, we used a model of Klebsiella pneumoniae in mice deficient in STAT6. We chose K. pneumoniae for our in vivo model, since K. pneumoniae increases IL-17A expression and γδ17 numbers. K. pneumoniae infection of STAT6 knockout mice resulted in a statistically significant increase in the number of γδ17 cells compared to that of wild-type mice. These studies are the first to demonstrate that γδ17 cells express the type I IL-4R and that STAT6 signaling negatively regulates γδ17 cells, a cell population that plays a front-line role in mucosal immunity.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Female
  • Immunity, Mucosal
  • Interleukin-17 / metabolism*
  • Interleukin-4 / metabolism
  • Klebsiella Infections / pathology*
  • Klebsiella pneumoniae / immunology*
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Receptors, Cell Surface / metabolism
  • STAT6 Transcription Factor / metabolism*
  • Signal Transduction*
  • T-Lymphocyte Subsets / immunology*
  • Th17 Cells / immunology*

Substances

  • Il4ra protein, mouse
  • Interleukin-17
  • Receptors, Cell Surface
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • Interleukin-4