Gp96 deficiency affects TLR4 functionality and impairs ERK and p38 phosphorylation

PLoS One. 2018 Feb 15;13(2):e0193003. doi: 10.1371/journal.pone.0193003. eCollection 2018.

Abstract

Gp96 is an endoplasmic reticulum chaperone for multiple protein substrates. Its lack in intestinal macrophages of Crohn's disease (CD) patients is correlated with loss of tolerance against the host gut flora. Gp96 has been stablished to be an essential chaperone for Toll-like receptors (TLRs). We studied the impact of gp96-knockdown on TLR-function in macrophages. TLR2 and TLR4 expression was only decreased but not abolished when gp96 was knocked-down in cell lines, whereas in a monocyte/macrophage specific knock-out mouse model (LysMCre) TLR4 was abolished, while TLR2 was still present. Lipopolysaccharide (LPS)-induced NF-κB activation was still observed in the absence of gp96, and gp96-deficient macrophages were able to up-regulate surface TLR4 upon LPS treatment, suggesting that there is another chaperone involved in the folding of TLR4 upon stress responses. Moreover, LPS-dependent pro-inflammatory cytokines were still expressed, although to a lesser extent in the absence of gp96, which reinforces the fact that gp96 is involved in regulating signaling cascades downstream of TLR4 are impaired upon loss of gp96. In addition, we have also found a reduced phosphorylation of ERK and p38 kinases and an impaired response upon CSF1R activation in gp96 deficient macrophages. Our findings indicate that the loss of gp96 not only impairs TLR4 signaling, but is also associated with a diminished phosphorylation of ERK and mitogen-activated stress kinases resulting in an impaired signalling through several receptors, including CSF1R.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • HEK293 Cells
  • Humans
  • Interleukin-8 / metabolism
  • Membrane Glycoproteins / deficiency*
  • Membrane Glycoproteins / genetics
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • NF-KappaB Inhibitor alpha / metabolism
  • NF-kappa B / metabolism
  • Phosphorylation / physiology
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / metabolism
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Interleukin-8
  • Membrane Glycoproteins
  • NF-kappa B
  • TLR2 protein, human
  • TLR4 protein, human
  • Tlr2 protein, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 2
  • Toll-Like Receptor 4
  • endoplasmin
  • NF-KappaB Inhibitor alpha
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases

Grants and funding

This research was funded by research grants from the Swiss National Science Foundation (Grant No. 310030_138410 and 310030-120312 to GR and Grant No. 31003A_127247 to MH), as well as the Swiss IBD Cohort (Grant No. 3347CO-108792) J. CR is supported by the ECCO Fellowship from European Crohn’s and Colitis Organisation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.