Regulation of T Cell Receptor Signaling by DENND1B in TH2 Cells and Allergic Disease

Cell. 2016 Jan 14;164(1-2):141-155. doi: 10.1016/j.cell.2015.11.052. Epub 2016 Jan 7.

Abstract

The DENN domain is an evolutionary conserved protein module found in all eukaryotes and serves as an exchange factor for Rab-GTPases to regulate diverse cellular functions. Variants in DENND1B are associated with development of childhood asthma and other immune disorders. To understand how DENND1B may contribute to human disease, Dennd1b(-/-) mice were generated and exhibit hyper-allergic responses following antigen challenge. Dennd1b(-/-) TH2, but not other TH cells, exhibit delayed receptor-induced T cell receptor (TCR) downmodulation, enhanced TCR signaling, and increased production of effector cytokines. As DENND1B interacts with AP-2 and Rab35, TH2 cells deficient in AP-2 or Rab35 also exhibit enhanced TCR-mediated effector functions. Moreover, human TH2 cells carrying asthma-associated DENND1B variants express less DENND1B and phenocopy Dennd1b(-/-) TH2 cells. These results provide a molecular basis for how DENND1B, a previously unrecognized regulator of TCR downmodulation in TH2 cells, contributes to asthma pathogenesis and how DENN-domain-containing proteins may contribute to other human disorders.

MeSH terms

  • Animals
  • Asthma / immunology*
  • Cytokines / genetics
  • Cytokines / immunology
  • Death Domain Receptor Signaling Adaptor Proteins / metabolism*
  • Dendritic Cells / immunology
  • Female
  • Guanine Nucleotide Exchange Factors / genetics
  • Guanine Nucleotide Exchange Factors / metabolism*
  • Humans
  • Hypersensitivity / immunology
  • Lymphocyte Activation
  • Mice
  • Polymorphism, Single Nucleotide
  • Receptors, Antigen, T-Cell / metabolism*
  • Signal Transduction*
  • Th2 Cells / immunology*
  • Th2 Cells / metabolism
  • rab GTP-Binding Proteins / genetics

Substances

  • Cytokines
  • DENND1B protein, human
  • DENND1B protein, mouse
  • Death Domain Receptor Signaling Adaptor Proteins
  • Guanine Nucleotide Exchange Factors
  • Receptors, Antigen, T-Cell
  • Rab35 protein, mouse
  • rab GTP-Binding Proteins