Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces

Background: The larval stages of Echinococcus granulosus sensu lato (E. granulosus s.l) infection can alter B cell function and affect host anti-infective immunity, but the underlying mechanism remains unclear. The newly emerging immunometabolism highlights that several metabolites are key factors i...

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Main Authors: Yuxin Guo, Daxiang Xu, Zheng Fang, Shiping Xu, Jiaxi Liu, Zixuan Xu, Jikai Zhou, Zhenzhen Bu, Yingyi Zhao, Jingmei He, Xiaoying Yang, Wei Pan, Yujuan Shen, Fenfen Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2021.718743/full
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author Yuxin Guo
Yuxin Guo
Yuxin Guo
Daxiang Xu
Zheng Fang
Zheng Fang
Zheng Fang
Shiping Xu
Shiping Xu
Shiping Xu
Jiaxi Liu
Jiaxi Liu
Jiaxi Liu
Zixuan Xu
Zixuan Xu
Zixuan Xu
Jikai Zhou
Jikai Zhou
Jikai Zhou
Zhenzhen Bu
Zhenzhen Bu
Zhenzhen Bu
Yingyi Zhao
Yingyi Zhao
Yingyi Zhao
Jingmei He
Xiaoying Yang
Xiaoying Yang
Wei Pan
Wei Pan
Yujuan Shen
Fenfen Sun
Fenfen Sun
author_facet Yuxin Guo
Yuxin Guo
Yuxin Guo
Daxiang Xu
Zheng Fang
Zheng Fang
Zheng Fang
Shiping Xu
Shiping Xu
Shiping Xu
Jiaxi Liu
Jiaxi Liu
Jiaxi Liu
Zixuan Xu
Zixuan Xu
Zixuan Xu
Jikai Zhou
Jikai Zhou
Jikai Zhou
Zhenzhen Bu
Zhenzhen Bu
Zhenzhen Bu
Yingyi Zhao
Yingyi Zhao
Yingyi Zhao
Jingmei He
Xiaoying Yang
Xiaoying Yang
Wei Pan
Wei Pan
Yujuan Shen
Fenfen Sun
Fenfen Sun
author_sort Yuxin Guo
collection DOAJ
description Background: The larval stages of Echinococcus granulosus sensu lato (E. granulosus s.l) infection can alter B cell function and affect host anti-infective immunity, but the underlying mechanism remains unclear. The newly emerging immunometabolism highlights that several metabolites are key factors in determining the fate of immune cells, which provides a new insight for exploring how larval E. granulosus s.l. infection remodels B cell function. This study investigated the metabolomic profiles of B cells in mice infected with E. granulosus s.l. protoscoleces (PSC).Results:Total CD19+ B cells, purified from the spleen of infected mice, showed significantly increased production of IL-6, TNF-α, and IL-10 after exposure to LPS in vitro. Moreover, the mRNA expression of metabolism related enzymes in B cells was remarkably disordered post infection. In addition, differential metabolites were identified in B cells after infection. There were 340 differential metabolites (83 upregulated and 257 downregulated metabolites) identified in the positive ion model, and 216 differential metabolites (97 upregulated and 119 downregulated metabolites) identified in the negative ion mode. Among these, 64 differential metabolites were annotated and involved in 68 metabolic pathways, including thyroid hormone synthesis, the metabolic processes of glutathione, fructose, mannose, and glycerophospholipid. Furthermore, several differential metabolites such as glutathione, taurine, and inosine were validated to regulate the cytokine production in LPS stimulated B cells.Conclusion:Infection with the larval E. granulosus s.l. causes metabolic reprogramming in the intrinsic B cells of mice, which provides the first evidence for understanding the role and mechanism of B cells in parasite anti-infective immunity from the viewpoint of immunometabolism.
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spelling doaj.art-e8a2c873509e40f59606ba95c39d0f1f2022-12-21T18:34:22ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-09-01810.3389/fvets.2021.718743718743Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato ProtoscolecesYuxin Guo0Yuxin Guo1Yuxin Guo2Daxiang Xu3Zheng Fang4Zheng Fang5Zheng Fang6Shiping Xu7Shiping Xu8Shiping Xu9Jiaxi Liu10Jiaxi Liu11Jiaxi Liu12Zixuan Xu13Zixuan Xu14Zixuan Xu15Jikai Zhou16Jikai Zhou17Jikai Zhou18Zhenzhen Bu19Zhenzhen Bu20Zhenzhen Bu21Yingyi Zhao22Yingyi Zhao23Yingyi Zhao24Jingmei He25Xiaoying Yang26Xiaoying Yang27Wei Pan28Wei Pan29Yujuan Shen30Fenfen Sun31Fenfen Sun32Jiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaThe First Clinical Medical College, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaNational Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Chinese Center for Tropical Diseases Research, NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai, ChinaJiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, ChinaNational Experimental Teaching Demonstration Center of Basic Medicine, Xuzhou Medical University, Xuzhou, ChinaBackground: The larval stages of Echinococcus granulosus sensu lato (E. granulosus s.l) infection can alter B cell function and affect host anti-infective immunity, but the underlying mechanism remains unclear. The newly emerging immunometabolism highlights that several metabolites are key factors in determining the fate of immune cells, which provides a new insight for exploring how larval E. granulosus s.l. infection remodels B cell function. This study investigated the metabolomic profiles of B cells in mice infected with E. granulosus s.l. protoscoleces (PSC).Results:Total CD19+ B cells, purified from the spleen of infected mice, showed significantly increased production of IL-6, TNF-α, and IL-10 after exposure to LPS in vitro. Moreover, the mRNA expression of metabolism related enzymes in B cells was remarkably disordered post infection. In addition, differential metabolites were identified in B cells after infection. There were 340 differential metabolites (83 upregulated and 257 downregulated metabolites) identified in the positive ion model, and 216 differential metabolites (97 upregulated and 119 downregulated metabolites) identified in the negative ion mode. Among these, 64 differential metabolites were annotated and involved in 68 metabolic pathways, including thyroid hormone synthesis, the metabolic processes of glutathione, fructose, mannose, and glycerophospholipid. Furthermore, several differential metabolites such as glutathione, taurine, and inosine were validated to regulate the cytokine production in LPS stimulated B cells.Conclusion:Infection with the larval E. granulosus s.l. causes metabolic reprogramming in the intrinsic B cells of mice, which provides the first evidence for understanding the role and mechanism of B cells in parasite anti-infective immunity from the viewpoint of immunometabolism.https://www.frontiersin.org/articles/10.3389/fvets.2021.718743/fullEchinococcus granulosusB cellmetabolomicsimmunometabolismmetabolitemetabolic reprogramming
spellingShingle Yuxin Guo
Yuxin Guo
Yuxin Guo
Daxiang Xu
Zheng Fang
Zheng Fang
Zheng Fang
Shiping Xu
Shiping Xu
Shiping Xu
Jiaxi Liu
Jiaxi Liu
Jiaxi Liu
Zixuan Xu
Zixuan Xu
Zixuan Xu
Jikai Zhou
Jikai Zhou
Jikai Zhou
Zhenzhen Bu
Zhenzhen Bu
Zhenzhen Bu
Yingyi Zhao
Yingyi Zhao
Yingyi Zhao
Jingmei He
Xiaoying Yang
Xiaoying Yang
Wei Pan
Wei Pan
Yujuan Shen
Fenfen Sun
Fenfen Sun
Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
Frontiers in Veterinary Science
Echinococcus granulosus
B cell
metabolomics
immunometabolism
metabolite
metabolic reprogramming
title Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
title_full Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
title_fullStr Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
title_full_unstemmed Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
title_short Metabolomics Analysis of Splenic CD19+ B Cells in Mice Chronically Infected With Echinococcus granulosus sensu lato Protoscoleces
title_sort metabolomics analysis of splenic cd19 b cells in mice chronically infected with echinococcus granulosus sensu lato protoscoleces
topic Echinococcus granulosus
B cell
metabolomics
immunometabolism
metabolite
metabolic reprogramming
url https://www.frontiersin.org/articles/10.3389/fvets.2021.718743/full
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