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

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

doi:10.3389/fvets.2022.848458

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

Front Vet Sci. 2022 Apr 25:9:848458. doi: 10.3389/fvets.2022.848458. eCollection 2022.

Authors

Shiping Xu^{1

2

3}, Yuxin Guo^{1

2

3}, Tiancheng Luo^{1

2

3}, Pengfei Jiang^{1

3}, Ziyi Yan^{1

2

3}, Yan He^{1

2

3}, Linlin Fu¹, Hua Liu^{4

5

6

7}, Zixuan Gao⁸, Dingmin Wang^{1

2

3}, Zhengxiu Sun^{1

2

3}, Xiaoying Yang¹, Wei Pan¹, Fenfen Sun^{1

3}

Affiliations

¹ Jiangsu Key Laboratory of Immunity and Metabolism, Department of Pathogen Biology and Immunology, Xuzhou Medical University, Xuzhou, China.
² The First Clinical Medical College, Xuzhou Medical University, Xuzhou, China.
³ National Experimental Teaching Demonstration Center of Basic Medicine (Xuzhou Medical University), Xuzhou, China.
⁴ National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, China.
⁵ National Health Commission Key Laboratory of Parasite and Vector Biology, Shanghai, China.
⁶ World Health Organization Collaborating Centre for Tropical Diseases, Shanghai, China.
⁷ National Center for International Research on Tropical Diseases, Shanghai, China.
⁸ Department of Physiology, Xuzhou Medical University, Xuzhou, China.

Abstract

Background: We 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.

Methods: The 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.

Results: A 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.

Conclusions: The 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.

Keywords: B cells; Echinococcus granulosus; immune regulation; lipid metabolism; metabolic reprogramming; protoscoleces.