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      Transcriptomic responses of water buffalo liver to infection with the digenetic fluke Fasciola gigantica

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          Abstract

          Background

          Fasciola gigantica, the tropical liver fluke, infects buffaloes in Asian and African countries and causes significant economic losses and poses public health threat in these countries. However, little is known of the transcriptional response of buffaloes to infection with F. gigantica. The objective of the present study was to perform the first transcriptomic analysis of buffalo liver infected by F. gigantica. Understanding the mechanisms that underpin F. gigantica infection in buffaloes will contribute to our ability to control this parasite.

          Methods

          We challenged buffaloes with 500 viable F. gigantica metacercariae and collected liver samples through a time course at 3, 42 and 70 days post-infection (dpi). Then, we performed gene expression analysis on liver samples using RNA sequencing (RNA-Seq) Illumina technology and confirmed the RNA-Seq data by quantitative RT-PCR analysis.

          Results

          Totals of 496, 880 and 441 differentially expressed transcripts were identified in the infected livers at 3, 42 and 70 dpi, respectively. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that transcriptional changes in the liver of infected buffaloes evolve over the course of infection. The predominant response of buffaloes to infection was mediated by certain pathways, such as MHC antigen processing and presentation, Toll-like receptor 4 (TLR4), transforming growth factor beta (TGF-β), and the cytochrome P450. Hepatic drug metabolizing enzymes and bile secretion were also affected.

          Conclusions

          Fasciola gigantica can induce statistically significant and biologically plausible differences in the hepatic gene expression of infected buffaloes. These findings provide new insights into the response of buffaloes to F. gigantica over the course of infection, which may be useful in determining pathways that can modulate host-parasite interaction and thus potentially important for clearance of the parasite.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-017-1990-2) contains supplementary material, which is available to authorized users.

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          Most cited references57

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          Follicular B Helper T Cells Express Cxc Chemokine Receptor 5, Localize to B Cell Follicles, and Support Immunoglobulin Production

          Chemokines and their receptors have been identified as major regulators controlling the functional organization of secondary lymphoid organs. Here we show that expression of CXC chemokine receptor 5 (CXCR5), a chemokine receptor required for B cell homing to B cell follicles, defines a novel subpopulation of B helper T cells localizing to follicles. In peripheral blood these cells coexpress CD45RO and the T cell homing CC chemokine receptor 7 (CCR7). In secondary lymphoid organs, CD4+CXCR5+ cells lose expression of CCR7, which allows them to localize to B cell follicles and germinal centers where they express high levels of CD40 ligand (CD40L), a costimulatory molecule required for B cell activation and inducible costimulator (ICOS), a recently identified costimulatory molecule of the CD28 family. Thus, when compared with CD4+CD45RO+CXCR5− cells, CD4+CD45RO+CXCR5+ tonsillar T cells efficiently support the production of immunoglobulin (Ig)A and IgG. In contrast, analysis of the memory response revealed that long-lasting memory cells are found within the CD4+CD45RO+CXCR5− population, suggesting that CXCR5+CD4 cells represent recently activated effector cells. Based on the characteristic localization within secondary lymphoid organs, we suggest to term these cells “follicular B helper T cells” (TFH).
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            The known unknowns of antigen processing and presentation.

            The principal components of both MHC class I and class II antigen processing and presentation pathways are well known. In dendritic cells, these pathways are tightly regulated by Toll-like-receptor signalling and include features, such as cross-presentation, that are not seen in other cell types. However, the exact mechanisms involved in the subcellular trafficking of antigens remain poorly understood and in some cases are controversial. Recent data suggest that diverse cellular machineries, including autophagy, participate in antigen processing and presentation, although their relative contributions remain to be fully elucidated. Here, we highlight some emerging themes of antigen processing and presentation that we think merit further attention.
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              Structural determinants of Smad function in TGF-β signaling.

              Smad transcription factors are central to the signal transduction pathway that mediates the numerous effects of the transforming growth factor β (TGF-β) superfamily of cytokines in metazoan embryo development as well as in adult tissue regeneration and homeostasis. Although Smad proteins are conserved, recent genome-sequencing projects have revealed their sequence variation in metazoan evolution, human polymorphisms, and cancer. Structural studies of Smads bound to partner proteins and target DNA provide a framework for understanding the significance of these evolutionary and pathologic sequence variations. We synthesize the extant mutational and structural data to suggest how genetic variation in Smads may affect the structure, regulation, and function of these proteins. We also present a web application that compares Smad sequences and displays Smad protein structures and their disease-associated variants.
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                Author and article information

                Contributors
                kid372820378@163.com
                zhangxiaoxuan1988@126.com
                hany.elsheikha@nottingham.ac.uk
                hejunjun617@163.com
                739037313@qq.com
                zhengwenwubin@qq.com
                15193194055@163.com
                wyhuang@gxu.edu.cn
                guoaijiang@caas.cn
                xingquanzhu1@hotmail.com
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                1 February 2017
                1 February 2017
                2017
                : 10
                : 56
                Affiliations
                [1 ]ISNI 0000 0001 0018 8988, GRID grid.454892.6, , State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, ; Lanzhou, Gansu Province 730046 People’s Republic of China
                [2 ]ISNI 0000 0004 1936 8868, GRID grid.4563.4, , Faculty of Medicine and Health Sciences, School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, ; Loughborough, LE12 5RD UK
                [3 ]ISNI 0000 0001 2254 5798, GRID grid.256609.e, , College of Animal Science and Technology, Guangxi University, ; Nanning, Guangxi Zhuang Autonomous Region 530005 People’s Republic of China
                [4 ]Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu Province 225009 People’s Republic of China
                Article
                1990
                10.1186/s13071-017-1990-2
                5286860
                28143561
                8f7715af-860c-435a-b10a-f3e75b340892
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 November 2016
                : 18 January 2017
                Funding
                Funded by: National Key Basic Research Program (973 Program) of China
                Award ID: 2015CB150300
                Award Recipient :
                Funded by: the Fundamental Research Funds for Central Research Institutes of Public Interests
                Award ID: 1610312017022
                Award Recipient :
                Funded by: the Fundamental Research Funds of Chinese Academy of Agricultural Sciences
                Award ID: Y2016JC05
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Parasitology
                fasciola gigantica,immunomodulation,rna-sequencing,transcriptome,water buffalo
                Parasitology
                fasciola gigantica, immunomodulation, rna-sequencing, transcriptome, water buffalo

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