Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice

Abstract Background A fundamental tenet of the hygiene theory is the inverse association between helminth infections and the emergence of immune-mediated diseases. Research has been done to clarify the processes by which helminth-derived molecules can inhibit immunological disorders. This study aime...

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Main Authors: Jia Xu, Ye Yao, Qisheng Zhuang, Zixuan Li, Min Zhang, Shouan Wang, Hongxin Hu, Jianbin Ye
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-024-06656-0
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author Jia Xu
Ye Yao
Qisheng Zhuang
Zixuan Li
Min Zhang
Shouan Wang
Hongxin Hu
Jianbin Ye
author_facet Jia Xu
Ye Yao
Qisheng Zhuang
Zixuan Li
Min Zhang
Shouan Wang
Hongxin Hu
Jianbin Ye
author_sort Jia Xu
collection DOAJ
description Abstract Background A fundamental tenet of the hygiene theory is the inverse association between helminth infections and the emergence of immune-mediated diseases. Research has been done to clarify the processes by which helminth-derived molecules can inhibit immunological disorders. This study aimed to evaluate the ability of Trichinella spiralis chitinase (Ts-chit) to ameliorate the symptoms of allergic airway inflammation. Methods Recombinant Trichinella spiralis chitinase (rTs-chit) was expressed in Escherichia coli BL21, and its structural homology to murine acidic mammalian chitinase (AMCase) was comprehensively analyzed. The expression of Ts-chit was examined across all T. spiralis life stages. To explore its immunomodulatory potential, a murine model of allergen-induced airway inflammation was established. The effects of rTs-chit were evaluated by assessing airway hyperresponsiveness and cytokine profiles in bronchoalveolar lavage fluid and performing detailed histopathological and immunohistochemical analyses. Results Recombinant Ts-chit (rTs-chit) was successfully expressed in E. coli BL21, showing strong structural similarity to murine acidic mammalian chitinase (AMCase). Expression profiling revealed that Ts-chit is present throughout all stages of the T. spiralis life cycle. In an allergic airway inflammation model, rTs-chit reduced weight loss and lung inflammation, lowering inflammatory cell infiltration and Th2 cytokines (IL-4, IL-5, IL-13) while increasing the immunosuppressive cytokine IL-10. Additionally, rTs-chit treatment decreased the expression of GATA3, arginase-1, MCP-1, CCL-11, and AMCase, along with reducing OVA-specific IgE, IgG, and IgG1 levels, suggesting its potential as an immunomodulatory agent. Conclusions This study highlights rTs-chit’s potential as a therapeutic agent for allergic airway diseases, leveraging its structural similarity to host chitinases to regulate Th2 responses and inflammatory pathways. The findings provide new insights into helminth-derived proteins as promising candidates for immune-based therapies. Graphical Abstract
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spelling doaj-art-0bdb508c480847c8ae6b4f64aff727b42025-01-19T12:12:07ZengBMCParasites & Vectors1756-33052025-01-0118111510.1186/s13071-024-06656-0Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in miceJia Xu0Ye Yao1Qisheng Zhuang2Zixuan Li3Min Zhang4Shouan Wang5Hongxin Hu6Jianbin Ye7School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in School of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in The Affiliated Hospital of Putian UniversitySchool of Basic Medicine Science, Fujian Province, Putian University, Key Laboratory of Translational Tumor Medicine in Abstract Background A fundamental tenet of the hygiene theory is the inverse association between helminth infections and the emergence of immune-mediated diseases. Research has been done to clarify the processes by which helminth-derived molecules can inhibit immunological disorders. This study aimed to evaluate the ability of Trichinella spiralis chitinase (Ts-chit) to ameliorate the symptoms of allergic airway inflammation. Methods Recombinant Trichinella spiralis chitinase (rTs-chit) was expressed in Escherichia coli BL21, and its structural homology to murine acidic mammalian chitinase (AMCase) was comprehensively analyzed. The expression of Ts-chit was examined across all T. spiralis life stages. To explore its immunomodulatory potential, a murine model of allergen-induced airway inflammation was established. The effects of rTs-chit were evaluated by assessing airway hyperresponsiveness and cytokine profiles in bronchoalveolar lavage fluid and performing detailed histopathological and immunohistochemical analyses. Results Recombinant Ts-chit (rTs-chit) was successfully expressed in E. coli BL21, showing strong structural similarity to murine acidic mammalian chitinase (AMCase). Expression profiling revealed that Ts-chit is present throughout all stages of the T. spiralis life cycle. In an allergic airway inflammation model, rTs-chit reduced weight loss and lung inflammation, lowering inflammatory cell infiltration and Th2 cytokines (IL-4, IL-5, IL-13) while increasing the immunosuppressive cytokine IL-10. Additionally, rTs-chit treatment decreased the expression of GATA3, arginase-1, MCP-1, CCL-11, and AMCase, along with reducing OVA-specific IgE, IgG, and IgG1 levels, suggesting its potential as an immunomodulatory agent. Conclusions This study highlights rTs-chit’s potential as a therapeutic agent for allergic airway diseases, leveraging its structural similarity to host chitinases to regulate Th2 responses and inflammatory pathways. The findings provide new insights into helminth-derived proteins as promising candidates for immune-based therapies. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06656-0ChitinaseTrichinella spiralisAsthmaAllergy
spellingShingle Jia Xu
Ye Yao
Qisheng Zhuang
Zixuan Li
Min Zhang
Shouan Wang
Hongxin Hu
Jianbin Ye
Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
Parasites & Vectors
Chitinase
Trichinella spiralis
Asthma
Allergy
title Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
title_full Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
title_fullStr Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
title_full_unstemmed Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
title_short Characterization of a chitinase from Trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
title_sort characterization of a chitinase from trichinella spiralis and its immunomodulatory effects on allergic airway inflammation in mice
topic Chitinase
Trichinella spiralis
Asthma
Allergy
url https://doi.org/10.1186/s13071-024-06656-0
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