Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes
Abstract Background Determining the mechanisms involved in the immune-pathogenesis of the tropical liver fluke, Fasciola gigantica, is crucial to the development of any effective therapeutic intervention. Here, we examined the differential gene expression of cytokines and transcription factors in th...
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doaj-9417b034c6f3439297f9cd3f569b4e252020-11-25T01:45:11ZengBMCParasites & Vectors1756-33052017-12-0110111210.1186/s13071-017-2538-1Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloesWei Shi0Zhi-Yong Wei1Hany M. Elsheikha2Fu-Kai Zhang3Zhao-An Sheng4Ke-Jing Lu5Dong-Ying Wang6Wei-Yi Huang7Xing-Quan Zhu8College of Animal Science and Technology, Guangxi UniversityCollege of Animal Science and Technology, Guangxi UniversityFaculty of Medicine and Health Sciences, School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington CampusState Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesCollege of Animal Science and Technology, Guangxi UniversityCollege of Animal Science and Technology, Guangxi UniversityCollege of Animal Science and Technology, Guangxi UniversityCollege of Animal Science and Technology, Guangxi UniversityState Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesAbstract Background Determining the mechanisms involved in the immune-pathogenesis of the tropical liver fluke, Fasciola gigantica, is crucial to the development of any effective therapeutic intervention. Here, we examined the differential gene expression of cytokines and transcription factors in the liver of F. gigantica-infected buffaloes, over the course of infection. Methods Water buffaloes (swamp type) were infected orally with 500 F. gigantica encysted metacercariae. Liver tissue samples were collected 3, 10, 28, 42, 70 and 98 days post-infection (dpi). Levels of gene expression of nine cytokines (IFN-γ, TGF-β, IL-1β, IL-4, IL-6, IL-10, IL-12B, IL-13 and IL-17A) and four transcription factors (T-bet, GATA-3, Foxp3 and ROR-γτ) were determined using quantitative real-time PCR (qRT-PCR). We evaluated any correlation between gene expression of these immune-regulatory factors and the severity of liver pathology. Results Histopathological examination revealed that cellular infiltration, hemorrhage and fibrosis without calcification in the liver parenchyma of infected buffaloes, increased over the course of infection. This progressive pathology was attributed to dysregulated and excessive inflammatory responses induced by infection. The early infection phase (3–10 dpi) was marked by a generalized immunosuppression and elevated TGF-β expression in order to facilitate parasite colonization. A mixed Th1/Th2 immune response was dominant from 28 to 70 dpi, to promote parasite survival while minimizing host tissue damage. During late infection (98 dpi), the response was biased towards Th1/Treg in order to inhibit the host’s Th2 protective response and promote chronic infection. Both IL-10 and IL-17A and the Th17/Treg balance, played key roles in mediating the inflammatory and immunoregulatory mechanisms in the liver during chronic fasciolosis. Conclusions Our data showed distinct CD4+ T helper (Th) polarization and cytokine dysregulation in response to F. gigantica infection in water buffaloes over the course of infection. Characterizing the temporal expression profiles for host immune genes during infection should provide important information for defining how F. gigantica adapts and survives in the liver of buffaloes and how host immune responses influence F. gigantica pathogenicity.http://link.springer.com/article/10.1186/s13071-017-2538-1Fasciola giganticaBuffaloesLiverCytokinesTranscription factorsGene expression |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Wei Shi Zhi-Yong Wei Hany M. Elsheikha Fu-Kai Zhang Zhao-An Sheng Ke-Jing Lu Dong-Ying Wang Wei-Yi Huang Xing-Quan Zhu |
spellingShingle |
Wei Shi Zhi-Yong Wei Hany M. Elsheikha Fu-Kai Zhang Zhao-An Sheng Ke-Jing Lu Dong-Ying Wang Wei-Yi Huang Xing-Quan Zhu Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes Parasites & Vectors Fasciola gigantica Buffaloes Liver Cytokines Transcription factors Gene expression |
author_facet |
Wei Shi Zhi-Yong Wei Hany M. Elsheikha Fu-Kai Zhang Zhao-An Sheng Ke-Jing Lu Dong-Ying Wang Wei-Yi Huang Xing-Quan Zhu |
author_sort |
Wei Shi |
title |
Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes |
title_short |
Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes |
title_full |
Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes |
title_fullStr |
Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes |
title_full_unstemmed |
Dynamic expression of cytokine and transcription factor genes during experimental Fasciola gigantica infection in buffaloes |
title_sort |
dynamic expression of cytokine and transcription factor genes during experimental fasciola gigantica infection in buffaloes |
publisher |
BMC |
series |
Parasites & Vectors |
issn |
1756-3305 |
publishDate |
2017-12-01 |
description |
Abstract Background Determining the mechanisms involved in the immune-pathogenesis of the tropical liver fluke, Fasciola gigantica, is crucial to the development of any effective therapeutic intervention. Here, we examined the differential gene expression of cytokines and transcription factors in the liver of F. gigantica-infected buffaloes, over the course of infection. Methods Water buffaloes (swamp type) were infected orally with 500 F. gigantica encysted metacercariae. Liver tissue samples were collected 3, 10, 28, 42, 70 and 98 days post-infection (dpi). Levels of gene expression of nine cytokines (IFN-γ, TGF-β, IL-1β, IL-4, IL-6, IL-10, IL-12B, IL-13 and IL-17A) and four transcription factors (T-bet, GATA-3, Foxp3 and ROR-γτ) were determined using quantitative real-time PCR (qRT-PCR). We evaluated any correlation between gene expression of these immune-regulatory factors and the severity of liver pathology. Results Histopathological examination revealed that cellular infiltration, hemorrhage and fibrosis without calcification in the liver parenchyma of infected buffaloes, increased over the course of infection. This progressive pathology was attributed to dysregulated and excessive inflammatory responses induced by infection. The early infection phase (3–10 dpi) was marked by a generalized immunosuppression and elevated TGF-β expression in order to facilitate parasite colonization. A mixed Th1/Th2 immune response was dominant from 28 to 70 dpi, to promote parasite survival while minimizing host tissue damage. During late infection (98 dpi), the response was biased towards Th1/Treg in order to inhibit the host’s Th2 protective response and promote chronic infection. Both IL-10 and IL-17A and the Th17/Treg balance, played key roles in mediating the inflammatory and immunoregulatory mechanisms in the liver during chronic fasciolosis. Conclusions Our data showed distinct CD4+ T helper (Th) polarization and cytokine dysregulation in response to F. gigantica infection in water buffaloes over the course of infection. Characterizing the temporal expression profiles for host immune genes during infection should provide important information for defining how F. gigantica adapts and survives in the liver of buffaloes and how host immune responses influence F. gigantica pathogenicity. |
topic |
Fasciola gigantica Buffaloes Liver Cytokines Transcription factors Gene expression |
url |
http://link.springer.com/article/10.1186/s13071-017-2538-1 |
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