Excretory/Secretory Products from Schistosoma japonicum Eggs Alleviate Ovalbumin-Induced Allergic Airway Inflammation

PLoS Negl Trop Dis. 2023 Oct 3;17(10):e0011625. doi: 10.1371/journal.pntd.0011625. eCollection 2023 Oct.

Abstract

Introduction: Excretory/secretory products (ESPs) derived from helminths have been reported to effectively control allergic inflammation, which have better therapeutic prospects than live parasite infections. However, it remains unknown whether ESPs from schistosome eggs can protect against allergies, despite reports alleging that schistosome infection could alleviate disordered allergic inflammation.

Method: In the present study, we investigated the protective effects of ESPs from Schistosoma japonicum eggs (ESP-SJE) on asthmatic inflammation. Firstly, we successfully established an allergic airway inflammation model in mice by alum-adjuvanted ovalbumin (OVA) sensitization and challenge. ESP-SJE were administered intraperitoneally on days -1 and 13 (before sensitization), on day 20 (before challenge), and on days 21-24 (challenge phase).

Results: The results showed that ESP-SJE treatment significantly reduced the infiltration of inflammatory cells, especially eosinophils into the lung tissue, inhibited the production of the total and OVA-specific IgE during OVA-sensitized and -challenged phases, respectively, and suppressed the secretion of Th2-type inflammatory cytokines (IL-4). Additionally, ESP-SJE treatment significantly upregulated the regulatory T cells (Tregs) in the lung tissue during OVA challenge. Furthermore, using liquid chromatography-mass spectrometry analysis and Treg induction experiments in vitro, we might identify nine potential therapeutic proteins against allergic inflammation in ESP-SJE. The targets of these candidate proteins included glutathione S-transferase, egg protein CP422 precursor, tubulin alpha-2/alpha-4 chain, actin-2, T-complex protein 1 subunit beta, histone H₄, whey acidic protein core region, and molecular chaperone HtpG.

Conclusion: Taken together, the results discussed herein demonstrated that ESP-SJE could significantly alleviate OVA-induced asthmatic inflammation in a murine model, which might be mediated by the upregulation of Treg in lung tissues that may be induced by the potential modulatory proteins. Therefore, potential proteins in ESP-SJE might be the best candidates to be tested for therapeutic application of asthma, thus pointing out to a possible new therapy for allergic airway inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asthma* / chemically induced
  • Asthma* / drug therapy
  • Bronchoalveolar Lavage Fluid
  • Cytokines
  • Disease Models, Animal
  • Egg Hypersensitivity*
  • Inflammation / drug therapy
  • Lung
  • Mice
  • Mice, Inbred BALB C
  • Ovalbumin / pharmacology
  • Ovalbumin / therapeutic use
  • Schistosoma japonicum*

Substances

  • Ovalbumin
  • Cytokines

Grants and funding

This work has been supported by funding from the National Natural Science Foundation of China (31725025 to WH), Shanghai Municipal Science and Technology Committee of Shanghai outstanding academic leaders plan (18XD1400400 to WH), Science and Technology Leading Talent Team in Inner Mongolia Autonomous Region (2022LJRC0009 to WH) of Wei Hu, who was this MS's corresponding author. The funder WH participates in study design, data collection and analysis, decision to publish, or preparation of the manuscript.