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Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis

Schistosoma parasites, causing schistosomiasis, exhibit typical host specificity in host preference. Many mammals, including humans, are susceptible to infection, while the widely distributed rodent, Microtus fortis, exhibits natural anti-schistosome characteristics. The mechanisms of host susceptib...

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Autores principales: Shen, Jia, Zhao, Siyu, Peng, Mei, Li, Yanguo, Zhang, Lichao, Li, Xiaoping, Hu, Yunyi, Wu, Mingrou, Xiang, Suoyu, Wu, Xiaoying, Liu, Jiahua, Zhang, Beibei, Chen, Zebin, Lin, Datao, Liu, Huanyao, Tang, Wenyan, Chen, Jun, Sun, Xi, Liao, Qi, Hide, Geoff, Zhou, Zhijun, Lun, Zhao-Rong, Wu, Zhongdao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Nature Singapore 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550985/
https://www.ncbi.nlm.nih.gov/pubmed/37794085
http://dx.doi.org/10.1038/s41421-023-00603-6
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author Shen, Jia
Zhao, Siyu
Peng, Mei
Li, Yanguo
Zhang, Lichao
Li, Xiaoping
Hu, Yunyi
Wu, Mingrou
Xiang, Suoyu
Wu, Xiaoying
Liu, Jiahua
Zhang, Beibei
Chen, Zebin
Lin, Datao
Liu, Huanyao
Tang, Wenyan
Chen, Jun
Sun, Xi
Liao, Qi
Hide, Geoff
Zhou, Zhijun
Lun, Zhao-Rong
Wu, Zhongdao
author_facet Shen, Jia
Zhao, Siyu
Peng, Mei
Li, Yanguo
Zhang, Lichao
Li, Xiaoping
Hu, Yunyi
Wu, Mingrou
Xiang, Suoyu
Wu, Xiaoying
Liu, Jiahua
Zhang, Beibei
Chen, Zebin
Lin, Datao
Liu, Huanyao
Tang, Wenyan
Chen, Jun
Sun, Xi
Liao, Qi
Hide, Geoff
Zhou, Zhijun
Lun, Zhao-Rong
Wu, Zhongdao
author_sort Shen, Jia
collection PubMed
description Schistosoma parasites, causing schistosomiasis, exhibit typical host specificity in host preference. Many mammals, including humans, are susceptible to infection, while the widely distributed rodent, Microtus fortis, exhibits natural anti-schistosome characteristics. The mechanisms of host susceptibility remain poorly understood. Comparison of schistosome infection in M. fortis with the infection in laboratory mice (highly sensitive to infection) offers a good model system to investigate these mechanisms and to gain an insight into host specificity. In this study, we showed that large numbers of leukocytes attach to the surface of human schistosomes in M. fortis but not in mice. Single-cell RNA-sequencing analyses revealed that macrophages might be involved in the cell adhesion, and we further demonstrated that M. fortis macrophages could be mediated to attach and kill schistosomula with dependence on Complement component 3 (C3) and Complement receptor 3 (CR3). Importantly, we provided direct evidence that M. fortis macrophages could destroy schistosomula by trogocytosis, a previously undescribed mode for killing helminths. This process was regulated by Ca(2+)/NFAT signaling. These findings not only elucidate a novel anti-schistosome mechanism in M. fortis but also provide a better understanding of host parasite interactions, host specificity and the potential generation of novel strategies for schistosomiasis control.
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spelling pubmed-105509852023-10-06 Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis Shen, Jia Zhao, Siyu Peng, Mei Li, Yanguo Zhang, Lichao Li, Xiaoping Hu, Yunyi Wu, Mingrou Xiang, Suoyu Wu, Xiaoying Liu, Jiahua Zhang, Beibei Chen, Zebin Lin, Datao Liu, Huanyao Tang, Wenyan Chen, Jun Sun, Xi Liao, Qi Hide, Geoff Zhou, Zhijun Lun, Zhao-Rong Wu, Zhongdao Cell Discov Article Schistosoma parasites, causing schistosomiasis, exhibit typical host specificity in host preference. Many mammals, including humans, are susceptible to infection, while the widely distributed rodent, Microtus fortis, exhibits natural anti-schistosome characteristics. The mechanisms of host susceptibility remain poorly understood. Comparison of schistosome infection in M. fortis with the infection in laboratory mice (highly sensitive to infection) offers a good model system to investigate these mechanisms and to gain an insight into host specificity. In this study, we showed that large numbers of leukocytes attach to the surface of human schistosomes in M. fortis but not in mice. Single-cell RNA-sequencing analyses revealed that macrophages might be involved in the cell adhesion, and we further demonstrated that M. fortis macrophages could be mediated to attach and kill schistosomula with dependence on Complement component 3 (C3) and Complement receptor 3 (CR3). Importantly, we provided direct evidence that M. fortis macrophages could destroy schistosomula by trogocytosis, a previously undescribed mode for killing helminths. This process was regulated by Ca(2+)/NFAT signaling. These findings not only elucidate a novel anti-schistosome mechanism in M. fortis but also provide a better understanding of host parasite interactions, host specificity and the potential generation of novel strategies for schistosomiasis control. Springer Nature Singapore 2023-10-05 /pmc/articles/PMC10550985/ /pubmed/37794085 http://dx.doi.org/10.1038/s41421-023-00603-6 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Shen, Jia
Zhao, Siyu
Peng, Mei
Li, Yanguo
Zhang, Lichao
Li, Xiaoping
Hu, Yunyi
Wu, Mingrou
Xiang, Suoyu
Wu, Xiaoying
Liu, Jiahua
Zhang, Beibei
Chen, Zebin
Lin, Datao
Liu, Huanyao
Tang, Wenyan
Chen, Jun
Sun, Xi
Liao, Qi
Hide, Geoff
Zhou, Zhijun
Lun, Zhao-Rong
Wu, Zhongdao
Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title_full Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title_fullStr Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title_full_unstemmed Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title_short Macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, Microtus fortis
title_sort macrophage-mediated trogocytosis contributes to destroying human schistosomes in a non-susceptible rodent host, microtus fortis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550985/
https://www.ncbi.nlm.nih.gov/pubmed/37794085
http://dx.doi.org/10.1038/s41421-023-00603-6
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