STAT5-induced lunatic fringe during Th2 development alters delta-like 4-mediated Th2 cytokine production in respiratory syncytial virus-exacerbated airway allergic disease

J Immunol. 2014 Feb 1;192(3):996-1003. doi: 10.4049/jimmunol.1301991. Epub 2013 Dec 23.

Abstract

Notch activation plays an important role in T cell development and mature T cell differentiation. In this study, we investigated the role of Notch activation in a mouse model of respiratory syncytial virus (RSV)-exacerbated allergic airway disease. During RSV exacerbation, in vivo neutralization of a specific Notch ligand, Delta-like ligand (Dll)-4, significantly decreased airway hyperreactivity, mucus production, and Th2 cytokines. Lunatic Fringe (Lfng), a glycosyltransferase that enhances Notch activation by Dll4, was increased during RSV exacerbation. Lfng loss of function in Th2-skewed cells inhibited Dll4-Notch activation and subsequent IL-4 production. Further knockdown of Lfng in T cells in CD4Cre(+)Lfng(fl/fl) mice showed reduced Th2 response and disease pathology during RSV exacerbation. Finally, we identified STAT5-binding cis-acting regulatory element activation as a critical driver of Lfng transcriptional activation. These data demonstrate that STAT5-dependent amplification of Notch-modifying Lfng augments Th2 response via Dll4 and is critical for amplifying viral exacerbation during allergic airway disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Allergens / immunology
  • Allergens / toxicity
  • Animals
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • Calcium-Binding Proteins
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Cockroaches
  • Cytokines / biosynthesis*
  • Cytokines / genetics
  • Disease Models, Animal
  • Glycosyltransferases / antagonists & inhibitors
  • Glycosyltransferases / biosynthesis
  • Glycosyltransferases / genetics
  • Glycosyltransferases / physiology*
  • Insect Proteins / immunology
  • Insect Proteins / toxicity
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Receptors, Notch / physiology
  • Respiratory Hypersensitivity / complications
  • Respiratory Hypersensitivity / immunology*
  • Respiratory Syncytial Virus Infections / complications
  • Respiratory Syncytial Virus Infections / immunology*
  • STAT5 Transcription Factor / antagonists & inhibitors
  • STAT5 Transcription Factor / immunology
  • STAT5 Transcription Factor / physiology*
  • Signal Transduction / immunology
  • Specific Pathogen-Free Organisms
  • Th2 Cells / immunology
  • Th2 Cells / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Allergens
  • Calcium-Binding Proteins
  • Cytokines
  • DLL4 protein, mouse
  • Insect Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Receptors, Notch
  • STAT5 Transcription Factor
  • Stat5a protein, mouse
  • Glycosyltransferases
  • Lfng protein, mouse