Toll-like receptor 4-, 7-, and 8-activated myeloid cells from patients with X-linked agammaglobulinemia produce enhanced inflammatory cytokines

J Allergy Clin Immunol. 2012 Jan;129(1):184-90.e1-4. doi: 10.1016/j.jaci.2011.10.009. Epub 2011 Nov 16.

Abstract

Background: Bruton tyrosine kinase (BTK) is a component of signaling pathways downstream from Toll-like receptors (TLRs) 2, 4, 7, 8, and 9. Previous work in BTK-deficient mice, cell lines, and cultured cells from patients with X-linked agammaglobulinemia (XLA) suggested defective TLR-driven cytokine production.

Objective: We sought to compare TLR-4-, TLR-7-, and TLR-8-induced cytokine production of primary cells from patients with XLA with that seen in control cells.

Methods: PBMCs from patients with XLA, freshly isolated plasmacytoid dendritic cells, monocytes, and monocytoid dendritic cells were activated with TLR-4, TLR-7, and TLR-8 agonists. Signaling intermediates and intracellular and secreted cytokine levels were compared with those seen in control cells.

Results: Although TLR-4, TLR-7, and TLR-8 activation of nuclear factor κB and mitogen-activated protein kinase pathways in cells from patients with XLA and control cells were comparable, TLR-activated freshly isolated monocytes and monocytoid dendritic cells from patients with XLA produced significantly more TNF-α, IL-6, and IL-10 than control cells. TLR-7/8-activated plasmacytoid dendritic cells produced normal amounts of IFN-α. In murine models BTK regulates the degradation of Toll-IL-1 receptor domain-containing adaptor protein, terminating TLR-4-induced cytokine production. Although this might explain the heightened TLR-4-driven cytokine production we observed, Toll-IL-1 receptor domain-containing adaptor protein degradation is intact in cells from patients with XLA, excluding this explanation.

Conclusion: In contrast to previous studies with BTK-deficient mice, cell lines, and cultured cells from patients with XLA suggesting impaired TLR-driven cytokine production, these data suggest that BTK inhibits TLR-induced cytokine production in primary human cells.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Agammaglobulinaemia Tyrosine Kinase
  • Agammaglobulinemia / immunology*
  • Amides / pharmacology
  • Child
  • Child, Preschool
  • Cytokines / biosynthesis*
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Genetic Diseases, X-Linked / immunology*
  • Humans
  • Infant
  • Inflammation Mediators / metabolism*
  • Male
  • Membrane Glycoproteins / metabolism
  • Mitogen-Activated Protein Kinases / metabolism
  • Monocytes / immunology
  • Monocytes / metabolism
  • Myeloid Cells / immunology*
  • NF-kappa B / metabolism
  • Nitriles / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Receptors, Interleukin-1 / metabolism
  • Signal Transduction
  • Toll-Like Receptor 4 / metabolism
  • Toll-Like Receptor 7 / metabolism
  • Toll-Like Receptor 8 / metabolism
  • Toll-Like Receptors / metabolism*
  • Young Adult

Substances

  • Amides
  • Cytokines
  • Inflammation Mediators
  • LFM A13
  • Membrane Glycoproteins
  • NF-kappa B
  • Nitriles
  • Protein Kinase Inhibitors
  • Receptors, Interleukin-1
  • TIRAP protein, human
  • TLR4 protein, human
  • TLR7 protein, human
  • TLR8 protein, human
  • Toll-Like Receptor 4
  • Toll-Like Receptor 7
  • Toll-Like Receptor 8
  • Toll-Like Receptors
  • Protein-Tyrosine Kinases
  • Agammaglobulinaemia Tyrosine Kinase
  • BTK protein, human
  • Btk protein, mouse
  • Mitogen-Activated Protein Kinases

Supplementary concepts

  • Bruton type agammaglobulinemia