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Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils

Upon encountering exogenous pathogens, polymorphonucleocytes (PMNs) engage in various processes to destroy them, including releasing neutrophil extracellular traps (NETs) that trap pathogens and induce phagocytosis and cytokine production. Parasites have unique strategies with which to evade the hos...

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Autores principales: Wang, Jing, Tang, Bin, You, Xihuo, Cai, Xuepeng, Jia, Wanzhong, Liu, Xiaolei, Liu, Mingyuan, Jin, Xuemin, Ding, Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588246/
https://www.ncbi.nlm.nih.gov/pubmed/37864246
http://dx.doi.org/10.1186/s13071-023-05979-8
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author Wang, Jing
Tang, Bin
You, Xihuo
Cai, Xuepeng
Jia, Wanzhong
Liu, Xiaolei
Liu, Mingyuan
Jin, Xuemin
Ding, Jing
author_facet Wang, Jing
Tang, Bin
You, Xihuo
Cai, Xuepeng
Jia, Wanzhong
Liu, Xiaolei
Liu, Mingyuan
Jin, Xuemin
Ding, Jing
author_sort Wang, Jing
collection PubMed
description Upon encountering exogenous pathogens, polymorphonucleocytes (PMNs) engage in various processes to destroy them, including releasing neutrophil extracellular traps (NETs) that trap pathogens and induce phagocytosis and cytokine production. Parasites have unique strategies with which to evade the host's immune response. However, the strategy employed by Trichinella spiralis in response to the reaction of PMNs has yet to be elucidated. This study explored the effect of excretory/secretory products (ESP) on three major functions: NETs, phagocytosis, and cytokine production. Specifically, PMNs were pre-treated with the ESP of 3-day-old adults and then stimulated with phorbol 12-myristate 13-acetate (PMA). We found that in PMNs pretreated with ESP, PMA-induced NET generation was suppressed by ESP. ROS production is a hallmark of PMA-induced NETosis. The LDH assay results showed that ESP inhibits NETs by suppressing ROS rather than promoting PMN death. Furthermore, ESP enhanced Escherichia coli engulfment by PMNs, improving overall phagocytic function. Finally, cytokine analysis revealed an increase in pro-inflammatory cytokine IL-1β, and other cytokines (IL-10, TNF-α), while IL-4 displayed a significant reduction. In conclusion, this study has unraveled T. spiralis' evasion and regulation mechanisms against innate immune cells, providing insights into parasite strategies to manipulate host immunity, potentially informing new treatments for NET-related autoimmune diseases. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05979-8.
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spelling pubmed-105882462023-10-21 Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils Wang, Jing Tang, Bin You, Xihuo Cai, Xuepeng Jia, Wanzhong Liu, Xiaolei Liu, Mingyuan Jin, Xuemin Ding, Jing Parasit Vectors Research Upon encountering exogenous pathogens, polymorphonucleocytes (PMNs) engage in various processes to destroy them, including releasing neutrophil extracellular traps (NETs) that trap pathogens and induce phagocytosis and cytokine production. Parasites have unique strategies with which to evade the host's immune response. However, the strategy employed by Trichinella spiralis in response to the reaction of PMNs has yet to be elucidated. This study explored the effect of excretory/secretory products (ESP) on three major functions: NETs, phagocytosis, and cytokine production. Specifically, PMNs were pre-treated with the ESP of 3-day-old adults and then stimulated with phorbol 12-myristate 13-acetate (PMA). We found that in PMNs pretreated with ESP, PMA-induced NET generation was suppressed by ESP. ROS production is a hallmark of PMA-induced NETosis. The LDH assay results showed that ESP inhibits NETs by suppressing ROS rather than promoting PMN death. Furthermore, ESP enhanced Escherichia coli engulfment by PMNs, improving overall phagocytic function. Finally, cytokine analysis revealed an increase in pro-inflammatory cytokine IL-1β, and other cytokines (IL-10, TNF-α), while IL-4 displayed a significant reduction. In conclusion, this study has unraveled T. spiralis' evasion and regulation mechanisms against innate immune cells, providing insights into parasite strategies to manipulate host immunity, potentially informing new treatments for NET-related autoimmune diseases. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05979-8. BioMed Central 2023-10-20 /pmc/articles/PMC10588246/ /pubmed/37864246 http://dx.doi.org/10.1186/s13071-023-05979-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wang, Jing
Tang, Bin
You, Xihuo
Cai, Xuepeng
Jia, Wanzhong
Liu, Xiaolei
Liu, Mingyuan
Jin, Xuemin
Ding, Jing
Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title_full Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title_fullStr Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title_full_unstemmed Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title_short Trichinella spiralis excretory/secretory products from adult worms inhibit NETosis and regulate the production of cytokines from neutrophils
title_sort trichinella spiralis excretory/secretory products from adult worms inhibit netosis and regulate the production of cytokines from neutrophils
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588246/
https://www.ncbi.nlm.nih.gov/pubmed/37864246
http://dx.doi.org/10.1186/s13071-023-05979-8
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