Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus

BackgroundWe previously reported that the larval Echinococcus granulosus (E. granulosus) infection can expand the population of regulatory B cells in mice, thereby inhibiting the anti-infective immunity. However, the underlying mechanism is still largely unknown. This study further investigated the...

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Main Authors: Shiping Xu, Yuxin Guo, Tiancheng Luo, Pengfei Jiang, Ziyi Yan, Yan He, Linlin Fu, Hua Liu, Zixuan Gao, Dingmin Wang, Zhengxiu Sun, Xiaoying Yang, Wei Pan, Fenfen Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2022.848458/full
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author Shiping Xu
Shiping Xu
Shiping Xu
Yuxin Guo
Yuxin Guo
Yuxin Guo
Tiancheng Luo
Tiancheng Luo
Tiancheng Luo
Pengfei Jiang
Pengfei Jiang
Ziyi Yan
Ziyi Yan
Ziyi Yan
Yan He
Yan He
Yan He
Linlin Fu
Hua Liu
Hua Liu
Hua Liu
Hua Liu
Zixuan Gao
Dingmin Wang
Dingmin Wang
Dingmin Wang
Zhengxiu Sun
Zhengxiu Sun
Zhengxiu Sun
Xiaoying Yang
Wei Pan
Fenfen Sun
Fenfen Sun
author_facet Shiping Xu
Shiping Xu
Shiping Xu
Yuxin Guo
Yuxin Guo
Yuxin Guo
Tiancheng Luo
Tiancheng Luo
Tiancheng Luo
Pengfei Jiang
Pengfei Jiang
Ziyi Yan
Ziyi Yan
Ziyi Yan
Yan He
Yan He
Yan He
Linlin Fu
Hua Liu
Hua Liu
Hua Liu
Hua Liu
Zixuan Gao
Dingmin Wang
Dingmin Wang
Dingmin Wang
Zhengxiu Sun
Zhengxiu Sun
Zhengxiu Sun
Xiaoying Yang
Wei Pan
Fenfen Sun
Fenfen Sun
author_sort Shiping Xu
collection DOAJ
description BackgroundWe previously reported that the larval Echinococcus granulosus (E. granulosus) infection can expand the population of regulatory B cells in mice, thereby inhibiting the anti-infective immunity. However, the underlying mechanism is still largely unknown. This study further investigated the holistic transcriptomic profiles of total splenic B cells following the chronic infection of the parasite.MethodsThe infection model of larval E. granulosus was established by intraperitoneal inoculation with 2000 protoscolexes. Magnetic-Activated Cell Separation (MACS) was used to isolate the total splenic B cells. RNA sequencing was performed to screen the differentially expressed genes (DEGs) after infection. The expression of selected DEGs was verified using qRT-PCR. Gene Ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, and Co-expression network analysis were applied to predict these DEGs' underlying biological processes, pathways, and interactions respectively.ResultsA total of 413 DEGs were identified in larval E. granulosus infected B cells, including 303 up- and 110 down-regulated genes. Notably, most DEGs related to inflammation and chemotaxis were significantly upregulated after infection. In line with these changes, significant expression upregulation of DEGs associated with fatty acid oxidation, lipid synthesis, lipolysis, lipid transport, and cholesterol biosynthesis, were observed in infected B cells. Co-expression network analysis showed an intimate interaction between these DEGs associated with immune and metabolism.ConclusionsThe present study revealed that the larval E. granulosus infection induces metabolic reprogramming of B cells, which provides a novel clue to clarify the immunoregulatory mechanism of B cells in parasitic infection.
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spelling doaj.art-ca2f573a97ae4b58be6c26c0983753762022-12-22T02:21:03ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692022-04-01910.3389/fvets.2022.848458848458Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosusShiping Xu0Shiping Xu1Shiping Xu2Yuxin Guo3Yuxin Guo4Yuxin Guo5Tiancheng Luo6Tiancheng Luo7Tiancheng Luo8Pengfei Jiang9Pengfei Jiang10Ziyi Yan11Ziyi Yan12Ziyi Yan13Yan He14Yan He15Yan He16Linlin Fu17Hua Liu18Hua Liu19Hua Liu20Hua Liu21Zixuan Gao22Dingmin Wang23Dingmin Wang24Dingmin Wang25Zhengxiu Sun26Zhengxiu Sun27Zhengxiu Sun28Xiaoying Yang29Wei Pan30Fenfen 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, 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, 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, ChinaNational Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization Collaborating Centre for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaDepartment of Physiology, 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, 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, ChinaBackgroundWe previously reported that the larval Echinococcus granulosus (E. granulosus) infection can expand the population of regulatory B cells in mice, thereby inhibiting the anti-infective immunity. However, the underlying mechanism is still largely unknown. This study further investigated the holistic transcriptomic profiles of total splenic B cells following the chronic infection of the parasite.MethodsThe infection model of larval E. granulosus was established by intraperitoneal inoculation with 2000 protoscolexes. Magnetic-Activated Cell Separation (MACS) was used to isolate the total splenic B cells. RNA sequencing was performed to screen the differentially expressed genes (DEGs) after infection. The expression of selected DEGs was verified using qRT-PCR. Gene Ontology (GO) analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, and Co-expression network analysis were applied to predict these DEGs' underlying biological processes, pathways, and interactions respectively.ResultsA total of 413 DEGs were identified in larval E. granulosus infected B cells, including 303 up- and 110 down-regulated genes. Notably, most DEGs related to inflammation and chemotaxis were significantly upregulated after infection. In line with these changes, significant expression upregulation of DEGs associated with fatty acid oxidation, lipid synthesis, lipolysis, lipid transport, and cholesterol biosynthesis, were observed in infected B cells. Co-expression network analysis showed an intimate interaction between these DEGs associated with immune and metabolism.ConclusionsThe present study revealed that the larval E. granulosus infection induces metabolic reprogramming of B cells, which provides a novel clue to clarify the immunoregulatory mechanism of B cells in parasitic infection.https://www.frontiersin.org/articles/10.3389/fvets.2022.848458/fullEchinococcus granulosusprotoscolecesB cellsimmune regulationmetabolic reprogramminglipid metabolism
spellingShingle Shiping Xu
Shiping Xu
Shiping Xu
Yuxin Guo
Yuxin Guo
Yuxin Guo
Tiancheng Luo
Tiancheng Luo
Tiancheng Luo
Pengfei Jiang
Pengfei Jiang
Ziyi Yan
Ziyi Yan
Ziyi Yan
Yan He
Yan He
Yan He
Linlin Fu
Hua Liu
Hua Liu
Hua Liu
Hua Liu
Zixuan Gao
Dingmin Wang
Dingmin Wang
Dingmin Wang
Zhengxiu Sun
Zhengxiu Sun
Zhengxiu Sun
Xiaoying Yang
Wei Pan
Fenfen Sun
Fenfen Sun
Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
Frontiers in Veterinary Science
Echinococcus granulosus
protoscoleces
B cells
immune regulation
metabolic reprogramming
lipid metabolism
title Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
title_full Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
title_fullStr Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
title_full_unstemmed Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
title_short Transcriptomic Profiles of Splenic CD19+ B Cells in Mice Chronically Infected With the Larval Echinococcus granulosus
title_sort transcriptomic profiles of splenic cd19 b cells in mice chronically infected with the larval echinococcus granulosus
topic Echinococcus granulosus
protoscoleces
B cells
immune regulation
metabolic reprogramming
lipid metabolism
url https://www.frontiersin.org/articles/10.3389/fvets.2022.848458/full
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