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

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

Gene expression response to a nematode parasite in novel and native eel hosts

“…RNA‐seq studies of infection experiments on a range of species indicate that the number of affected processes, the magnitude of change, and the specific genes involved differ considerably among host species‐parasite species systems (e.g., Alvarez Rojas et al, ; Haase et al, ; Kumar, Abd‐Elfattah, & El‐Matbouli, ; Zhang et al, ). Infections with invasive parasites have consistently induced a more pronounced response in susceptible hosts compared with resistant hosts.…”

“…Differential regulation of processes associated with both the innate and the adaptive immune system in immune organs and at the site of infection is a common feature in natural and experimental infections in vertebrates (e.g., Alvarez Rojas et al, 2015;Babayan et al, 2018;Huang et al, 2016) and the gradual shift from the regulation of innate to adaptive immune processes can be observed in gene expression studies (Ehret, Spork, Dieterich, Lucius, & Heitlinger, 2017). Additionally, parasite infections cause differential expression of genes not directly related to an immune response, such as those involved in metabolic processes, tissue repair, or organ function and development (Alvarez Rojas et al, 2015;Babayan et al, 2018;Ronza et al, 2016;Zhang et al, 2017) and this has also been observed in the European eel Schneebauer et al, 2017). How A. crassus affects gene expression in the Japanese eel and what processes are modified upon infection have not yet been determined for any parasitic stage.…”

Modulation of the Functions of Goat Peripheral Blood Mononuclear Cells by Fasciola gigantica Thioredoxin Peroxidase In Vitro

“…The increased level of the proinflammatory cytokine IL-17 indicates that IL-17 and Th17 contribute to immunoregulatory mechanisms during F. gigantica infection. In the course of our previous research, a modest Th2 response at the early stage of infection was found to balance harmful Th1 and Th17 responses in F. gigantica -infected buffaloes [ 46 ]. We also observed that F. gigantica infection had a significant impact on the expression of Th1, Th2, Th17, and Treg cytokines [ 47 ].…”

A recombinant Fasciola gigantica 14-3-3 epsilon protein (rFg14-3-3e) modulates various functions of goat peripheral blood mononuclear cells

“…An ‘early’ TGF-β-associated immuno-suppressive response together with upregulation of liver IL-10 mRNA expression [ 52 ] and increased level of serum IL-10 cytokine [ 53 ] have been observed in buffaloes during early F. gigantica infection. In another study, we reported downregulation of MHC-II related genes and suppression of the host pro-inflammatory (Th1) immune response during early F. gigantica infection in buffalo liver [ 54 ]. This observation extends to F. hepatica , where immunosuppression, mediated by IL-4 and IL-10, was reported in experimentally infected rats during the early stage of liver penetration [ 55 ].…”