The Synergy of Endotoxin and (1→3)-β-D-Glucan, from Gut Translocation, Worsens Sepsis Severity in a Lupus Model of Fc Gamma Receptor IIb-Deficient Mice

J Innate Immun. 2018;10(3):189-201. doi: 10.1159/000486321. Epub 2018 Jan 31.

Abstract

We investigated the influence of spontaneous gut leakage upon polymicrobial sepsis in a lupus model with Fc gamma receptor IIb-deficient (FcGRIIb-/-) mice aged 8 and 40 weeks, as representing asymptomatic and symptomatic lupus, respectively. Spontaneous gut leakage, determined by (i) the presence of FITC-dextran, (ii) elevated serum endotoxin, and (iii) elevated serum (1→3)-β-D-glucan (BG), was demonstrated in symptomatic lupus but not in the asymptomatic group. In parallel, spontaneous gut leakage, detected by elevated serum BG without fungal infection, was demonstrated in patients with active lupus nephritis. Gut leakage induced by dextran sulfate solution (DSS) or endotoxin administration together with BG or endotoxin alone, but not BG alone, enhanced the severity of cecal ligation and puncture (CLP) sepsis more prominently in 8-week-old FcGRIIb-/- mice. Additionally, the bone marrow-derived macrophages of FcGRIIb-/- mice produced higher cytokine levels when coexposed to endotoxin and BG, when compared to wild-type mice. In summary, spontaneous gut leakage was demonstrated in symptomatic FcGRIIb-/- mice and the induction of gut permeability worsened sepsis severity. Gut translocation of endotoxin and BG had a minor effect on wild-type mice, but the synergistic effect of BG and endotoxin was prominent in FcGRIIb-/- mice. The data suggest that therapeutic strategies addressing gut leakage may be of interest in sepsis conditions in patients with lupus.

Keywords: (1→3)-β-D-glucan; Endogenous endotoxin; FcGRIIb-deficient mice; Sepsis severity; Systemic lupus erythematosus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Cytokines / blood
  • Cytokines / metabolism
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Endotoxins / blood*
  • Endotoxins / metabolism
  • Female
  • Gastrointestinal Tract / drug effects
  • Gastrointestinal Tract / metabolism
  • Humans
  • Lupus Erythematosus, Systemic / blood
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / pathology
  • Lupus Nephritis / blood
  • Lupus Nephritis / immunology
  • Lupus Nephritis / pathology
  • Macrophages / metabolism
  • Mice
  • Permeability / drug effects
  • Proteoglycans
  • Receptors, IgG / deficiency
  • Sepsis / blood*
  • Sepsis / immunology
  • Sepsis / pathology*
  • Survival Analysis
  • beta-Glucans / blood*
  • beta-Glucans / metabolism

Substances

  • Cytokines
  • Endotoxins
  • Fc gamma receptor IIB
  • Proteoglycans
  • Receptors, IgG
  • beta-Glucans
  • polysaccharide-K
  • Dextran Sulfate