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Comprehensive Analyses of circRNA Expression Profiles and Function Prediction in Chicken Cecums After Eimeria tenella Infection.

ABSTRACT: Coccidiosis is an important intestinal parasitic disease that causes great economic losses to the global poultry production industry. Circular RNAs (circRNAs) are long non-coding RNAs that play important roles in various infectious diseases and inflammatory responses. However, the expression profiles and functions of circRNAs during Eimeria tenella (E. tenella) infection remain unclear. In this study, high-throughput sequencing was carried out to detect circRNAs in chicken cecal tissues from the control (JC), resistant (JR), and susceptible (JS) groups on day 4.5 postinfection (pi), respectively. A total of 104 circRNAs were differentially expressed, including 47 circRNAs between the JS and JC groups, 38 between the JR and JS groups, and 19 between the JR and JC groups. Functional analyses indicated that these differentially expressed circRNAs were involved in pathways related to E. tenella infection; the adaptive immune response was enriched in the JS vs JC group, the NF-kappa B signaling and natural killer cell-mediated cytotoxicity pathways were enriched in the JS vs JC and JR vs JC groups, while the B cell receptor signaling pathway was enriched in only the JR vs JC group. Moreover, the coexpression network of differentially expressed circRNAs and mRNAs suggested that circRNA2202 and circRNA0759 associated with DTX1 in the JS vs JC group, circRNA4338 associated with VPREB3 and CXCL13L3 in the JR vs JC group, and circRNA2612 associated with IL8L1 and F2RL2 in the JR vs JS group were involved in the immune response upon E. tenella infection. In conclusion, our results provide valuable information on the circRNAs involved in the progression of chicken E. tenella infection and advance our understanding of the circRNA regulatory mechanisms of host resistance and susceptibility to E. tenella infection in chickens.

SUBMITTER: Yu H

PROVIDER: S-EPMC7988198 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Eimeria species cause the intestinal disease coccidiosis, most notably in poultry. While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible exception of Clostridium perfringens (necrotic enteritis). This study evaluated the composition and structure of the caecal microbiome in the presence or absence of a defined Eimeria tenella challenge infection in Cobb500 broiler chickens using 16S rRNA amplicon sequencing. The severity of clinical coccidiosis in individual chickens was quantified by caecal lesion scoring and microbial changes associated with different lesion scores identified. Following E. tenella infection the diversity of taxa within the caecal microbiome remained largely stable. However, infection induced significant changes in the abundance of some microbial taxa. The greatest changes were detected in birds displaying severe caecal pathology; taxa belonging to the order Enterobacteriaceae were increased, while taxa from Bacillales and Lactobacillales were decreased with the changes correlated with lesion severity. Significantly different profiles were also detected in infected birds which remained asymptomatic (lesion score 0), with taxa belonging to the genera Bacteroides decreased and Lactobacillus increased. Many differential taxa from the order Clostridiales were identified, with some increasing and others decreasing in abundance in Eimeria-infected animals. The results support the view that caecal microbiome dysbiosis associated with Eimeria infection contributes to disease pathology, and could be a target for intervention to mitigate the impact of coccidiosis on poultry productivity and welfare. This work highlights that E. tenella infection has a significant impact on the abundance of some caecal bacteria with notable differences detected between lesion score categories emphasising the importance of accounting for differences in caecal lesions when investigating the relationship between E. tenella and the poultry intestinal microbiome.

Project description:BackgroundChicken coccidiosis, a disease caused by seven species of Eimeria (Apicomplexa: Coccidia), inflicts severe economic losses on the poultry industry. Eimeria tenella is the one of the most virulent species pathogenic to chickens. Many parasitic protozoans are parasitised by double-stranded (ds) RNA viruses, and the influence of protozoan viruses on parasitic protozoans has been extensively reported. E. tenella RNA virus 1 (Etv) was identified in E. tenella, and the complete genome sequence of Etv was analysed. Here, we screened Etv-RNA-dependent RNA polymerase (RDRP)-interacting host protein E. tenella ovarian tumour (OTU) protein-like cysteine protease (Et-OTU) using a yeast two-hybrid system with pGBKT7-RDRP plasmid serving as bait. A previous study demonstrated that Et-OTU could regulate the telomerase activity of E. tenella, indicating that Et-OTU affects E. tenella proliferation. However, whether Etv-RDRP affects the molecular biological characteristics of E. tenella by interacting with OTU remains unclear.ResultsWe obtained seven positive clones from the initial screen, and six of the seven preys were identified as false-positives. Finally, we identified an RDRP-associated protein predicted to be an E. tenella OTU protein. A α-galactosidase assay showed that the bait vector did not activate the GAL4 reporter gene, indicating no autoactivation activity from the RDRP bait fusion. Pull-down and co-immunoprecipitation assays verified the interaction between Et-OTU and Etv-RDRP both intracellularly and extracellularly. Additionally, Et-OTU was able to deconjugate K48- and K6-linked di-ubiquitin (di-Ub) chains in vitro but not K63-, K11-, K29-, or K33-linked di-Ub chains. The C239A and H351A mutations eliminated the deubiquitinase (DUB) activity of Et-OTU, whereas the D236A mutation did not. Additionally, when combined with RDRP, the DUB activity of Et-OTU towards K48- and K6-linked chains was significantly enhanced.ConclusionEtv-RDRP interacts with Et-OTU both intracellularly and extracellularly. Etv-RDRP enhances the hydrolysis of Et-OTU to K6- or K48-linked ubiquitin chains. This study lays the foundation for further research on the relationship between E. tenella and Etv.

Project description:The T cell-mediated immune response plays an important role in coccidiosis. To reveal the host T cell immune response following Eimeria tenella (E. tenella) infection in chickens, we performed quantitative real-time PCR to analyze the dynamic expression of the Th1-related cytokines IFN-γ, IL-2, and IL-12; the Th17-related cytokines IL-17A, IL-17F, and IL-22; and the Treg-related cytokines IL-10, TGF-β, and CTLA-4 in the cecum and spleen at 0, 2, 4, 6, 8, and 10 d postinfection (dpi). In the cecal tissue, the expression of the Th1-related cytokine IFN-γ was significantly higher at 6 and 8 dpi than at other time points (11.97-fold and 39.78-fold, respectively, compared with 0 dpi, P < 0.05). IL-2 and IL-12 expression was significantly higher at 6 and 8 dpi than at 0, 2 and 10 dpi (P < 0.05). The expression of the Th17-related cytokines IL-17A and IL-17F at 2 and 4 dpi and IL-22 expression at 4 dpi were significantly higher than those at 0, 6, 8 and 10 dpi (P < 0.05). The expression of the Treg-related cytokines IL-10, TGF-β and CTLA-4 was significantly higher at 6 and 8 dpi than at 0, 2 and 4 dpi (P < 0.05). In the spleen, IFN-γ and IL-12 expression peaked at 4 dpi, while IL-2 expression peaked at 10 dpi. IL-17A, IL-17F and IL-22 expression was significantly higher at 2 and 4 dpi than at 0, 6, 8 and 10 dpi (P < 0.05). Treg-related cytokine TGF-β expression was almost unchanged and significantly decreased at only 4 dpi (P < 0.05), while CTLA-4 expression showed an overall decreasing trend from 0 to 8 dpi but increased significantly at 10 dpi (P < 0.05). The expression patterns of three T cell subset-related cytokines were different in the cecum and spleen. Furthermore, Th1 and Treg cells participate in the immune response mainly in the latter stage of coccidia infection (6 and 8 dpi), while Th17 cells play a role mainly in the early stages of infection (2 and 4 dpi). Our data will help to deepen the understanding of the complex T cell immune response after coccidia infection.

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Comprehensive Analyses of circRNA Expression Profiles and Function Prediction in Chicken Cecums After Eimeria tenella Infection.

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