TLR4 induced Wnt3a-Dvl3 restrains the intensity of inflammation and protects against endotoxin-driven organ failure through GSK3β/β-catenin signaling

Mol Immunol. 2020 Feb:118:153-164. doi: 10.1016/j.molimm.2019.12.013. Epub 2019 Dec 26.

Abstract

Background: Accumulating evidence suggests a regulatory role of Wnt proteins in innate immune responses. However, the effects of Wnt3a signaling on TLR4-mediated inflammatory responses are controversial and the signaling crosstalk between TLR4 and Wnt3a remains uncertain.

Methods: Gain- and Loss- of function approaches were utilized to determine the function of Wnt3a signaling in TLR4-mediated inflammatory responses. Cytokine production at protein and mRNA levels and phosphorylation of signaling molecules were measured by ELISA, qRT-PCR, and Western Blot, respectively. Endotoxemia mouse model was employed to assess the effect of Wnt3a on systemic inflammatory cytokine levels and neutrophil infiltration.

Results: LPS stimulation leads to an increase of Wnt3a expression and its downstream molecule, Dvl3, in primary monocytes. Inhibition or silence of Wnt3a or Dvl3 significantly increases the production of pro-inflammatory cytokines (IL-12, IL-6, TNFα), robustly reduces β-catenin accumulation, and enhances the phosphorylation of NF-κB P65 and its DNA binding activity. These results were confirmed by multiple gain- and loss- of function approaches including specific siRNA and ectopic expression of Dvl3, GSK3β, and β-catenin in monocytes. Moreover, in vivo relevance was established in a murine endotoxin model, in which Wnt3a inhibition enhances the inflammatory responses by augmenting the systemic pro-inflammatory cytokine levels and neutrophil infiltration.

Conclusions: TLR4 activation promotes Wnt3a-Dvl3 signaling, which acts as rheostats to restrain the intensity of inflammation through regulating GSK3β-β-catenin signaling and NF-κB activity.

General significance: Wnt3a-Dvl3-β-catenin signaling axis could be a potential interventional target for manipulating the direction and intensity of inflammatory responses.

Keywords: Dvl3; Inflammation regulation; TLR4; Wnt3; β-catenin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cytokines / metabolism
  • Dishevelled Proteins / metabolism*
  • Endotoxins / metabolism
  • Glycogen Synthase Kinase 3 beta / metabolism*
  • Humans
  • Inflammation / metabolism*
  • Lipopolysaccharides / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / metabolism
  • Multiple Organ Failure / metabolism
  • Phosphorylation / physiology
  • Signal Transduction / physiology*
  • Toll-Like Receptor 4 / metabolism*
  • Transcription Factor RelA / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Wnt3A Protein / metabolism*
  • beta Catenin / metabolism*

Substances

  • Cytokines
  • Dishevelled Proteins
  • Dvl3 protein, mouse
  • Endotoxins
  • Lipopolysaccharides
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Transcription Factor RelA
  • Tumor Necrosis Factor-alpha
  • Wnt3A Protein
  • Wnt3a protein, mouse
  • beta Catenin
  • Glycogen Synthase Kinase 3 beta