Soybean Agglutinin Alters the Gut Microbiota and Promotes Inflammation in Lupus-Prone MRL/lpr Mice

J Nutr. 2024 Mar;154(3):1039-1049. doi: 10.1016/j.tjnut.2024.01.015. Epub 2024 Jan 14.

Abstract

Background: Certain foods can trigger flares in patients with systemic lupus erythematosus. Lectins in edible plants have been reported to increase inflammation.

Objective: This study aimed to determine the effects of 1-time intake of soybean agglutinin (SBA) on the gut microbiota and immune response in lupus-prone MRL/MpJ (MRL)/lpr mice.

Methods: MRL/MpJ-Faslpr/J (MRL/lpr) and MRL mice were randomly assigned into 4 groups (8 mice/group): MRL mice + phosphate-buffered saline (PBS) (CON), MRL mice + SBA (CS), MRL/lpr mice + PBS (LPR), and MRL/lpr + SBA (LS). PBS and SBA were orally administered at 16 wk of age, and all mice were killed 24 h after oral challenge. The disease phenotype, levels of proinflammatory cytokines, and composition of the intestinal microbiota were determined.

Results: Interferon-gamma (IFN-γ) in the serum was significantly higher, whereas the level of serum IL-10 was significantly lower in LS mice than in LPR mice [fold change (FC) = 1.31 and FC = 0.36, respectively]. The expression levels of IL-6 and TNF-α in the spleen of LS mice were significantly higher than those in LPR mice (FC = 1.66 and FC = 1.96, respectively). The expression levels of IL-6, TNF-α, and IL-1β in the kidney were also significantly higher in LS mice than in LPR mice (FC = 2.89, FC = 3.78, and FC = 2.02, respectively). The relative abundances of Erysipelotrichaceae and Turicibacter in LS mice were significantly higher than those in LPR mice (FC = 1.73 and FC = 1.74, respectively). The percentage of Breg cells in the mesenteric lymph nodes was significantly lower in LS mice than in LPR mice (FC = 0.53) (P < 0.05). No change was found between SBA treatment or not in the control (MRL) mice.

Conclusions: One-time intake of SBA can promote the secretion of proinflammatory cytokines, downregulate Breg cells, and alter the intestinal flora in MRL/lpr mice within 24 h of oral challenge, which may contribute to exacerbation of lupus.

Keywords: Breg cells; Treg cells; gut microbiota; inflammatory factors; soybean agglutinin; systemic lupus erythematosus.

MeSH terms

  • Animals
  • Cytokines / metabolism
  • Gastrointestinal Microbiome*
  • Humans
  • Inflammation
  • Interleukin-6
  • Mice
  • Mice, Inbred MRL lpr
  • Phytohemagglutinins*
  • Soybean Proteins*
  • Tumor Necrosis Factor-alpha

Substances

  • soybean lectin
  • Interleukin-6
  • Tumor Necrosis Factor-alpha
  • Cytokines
  • Phytohemagglutinins
  • Soybean Proteins