Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)

Abstract Background Interferon (IFN) regulatory factors (IRFs) is a kind of transcription factors, which play an important role in regulating the expression of type I IFN and related genes. In mammals, IRF6 is not relevant with IFN expression, while zebrafish IRF6 was reported to be a positive regul...

Full description

Bibliographic Details
Main Authors: Yaxin Liang, Rongrong Liu, Jiahui Zhang, Yixin Chen, Shijuan Shan, Yaoyao Zhu, Guiwen Yang, Hua Li
Format: Article
Language:English
Published: BMC 2022-12-01
Series:BMC Veterinary Research
Subjects:
Online Access:https://doi.org/10.1186/s12917-022-03538-4
_version_ 1797980254905565184
author Yaxin Liang
Rongrong Liu
Jiahui Zhang
Yixin Chen
Shijuan Shan
Yaoyao Zhu
Guiwen Yang
Hua Li
author_facet Yaxin Liang
Rongrong Liu
Jiahui Zhang
Yixin Chen
Shijuan Shan
Yaoyao Zhu
Guiwen Yang
Hua Li
author_sort Yaxin Liang
collection DOAJ
description Abstract Background Interferon (IFN) regulatory factors (IRFs) is a kind of transcription factors, which play an important role in regulating the expression of type I IFN and related genes. In mammals, IRF6 is not relevant with IFN expression, while zebrafish IRF6 was reported to be a positive regulator of IFN expression and could be phosphorylated by both MyD88 and TBK1. However, the role of IRF6 in the immune response and IFN transcription of common carp is unknown. Results In the present study, the cDNA of IRF6 gene (CcIRF6) was cloned from common carp using RACE technique, with a total length of 1905 bp, encoding 471 amino acid residues, which possesses two functional domains of DBD and IAD. Similarity analysis showed that CcIRF6 had more than 50% similarity with IRFs of other vertebrates, and had the highest similarity with grass carp and zebrafish, among which the DBD domain was much more conserved. The phylogenetic analysis showed that CcIRF6 is in the branch of Osteichthyes and has the closest relationship with grass carp. In healthy common carp, the CcIRF6 was expressed in all the examined tissues, with the highest level in the oral epithelium, and the lowest level in the head kidney. After intraperitoneal injection of poly(I:C) or Aeromonas hydrophila, the expression of CcIRF6 increased in spleen, head kidney, foregut and hindgut of common carp. Moreover, poly(I:C), LPS, PGN and flagellin induced the expression of CcIRF6 in peripheral leukocytes and head kidney leukocytes of common carp in vitro. In EPC cells, CcIRF6 inhibited the expression of some IFN-related genes and pro-inflammatory cytokines, and dual luciferase reporter assay showed that CcIRF6 reduced the activity of IFN and NF-κB reporter genes. Conclusions The present study suggests that CcIRF6 is involved in the antiviral and antibacterial immune response of common carp, and negatively regulate the expression of IFN and NF-κB signalling pathways, which provides a theoretical basis for the study and prevention of fish disease pathogenesis.
first_indexed 2024-04-11T05:51:36Z
format Article
id doaj.art-ea28eb8bb5a84c43b59ebcb3bf863d48
institution Directory Open Access Journal
issn 1746-6148
language English
last_indexed 2024-04-11T05:51:36Z
publishDate 2022-12-01
publisher BMC
record_format Article
series BMC Veterinary Research
spelling doaj.art-ea28eb8bb5a84c43b59ebcb3bf863d482022-12-22T04:42:03ZengBMCBMC Veterinary Research1746-61482022-12-0118111210.1186/s12917-022-03538-4Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)Yaxin Liang0Rongrong Liu1Jiahui Zhang2Yixin Chen3Shijuan Shan4Yaoyao Zhu5Guiwen Yang6Hua Li7Shandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityCollege of Fisheries and Life Science, Hainan Tropical Ocean UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal UniversityAbstract Background Interferon (IFN) regulatory factors (IRFs) is a kind of transcription factors, which play an important role in regulating the expression of type I IFN and related genes. In mammals, IRF6 is not relevant with IFN expression, while zebrafish IRF6 was reported to be a positive regulator of IFN expression and could be phosphorylated by both MyD88 and TBK1. However, the role of IRF6 in the immune response and IFN transcription of common carp is unknown. Results In the present study, the cDNA of IRF6 gene (CcIRF6) was cloned from common carp using RACE technique, with a total length of 1905 bp, encoding 471 amino acid residues, which possesses two functional domains of DBD and IAD. Similarity analysis showed that CcIRF6 had more than 50% similarity with IRFs of other vertebrates, and had the highest similarity with grass carp and zebrafish, among which the DBD domain was much more conserved. The phylogenetic analysis showed that CcIRF6 is in the branch of Osteichthyes and has the closest relationship with grass carp. In healthy common carp, the CcIRF6 was expressed in all the examined tissues, with the highest level in the oral epithelium, and the lowest level in the head kidney. After intraperitoneal injection of poly(I:C) or Aeromonas hydrophila, the expression of CcIRF6 increased in spleen, head kidney, foregut and hindgut of common carp. Moreover, poly(I:C), LPS, PGN and flagellin induced the expression of CcIRF6 in peripheral leukocytes and head kidney leukocytes of common carp in vitro. In EPC cells, CcIRF6 inhibited the expression of some IFN-related genes and pro-inflammatory cytokines, and dual luciferase reporter assay showed that CcIRF6 reduced the activity of IFN and NF-κB reporter genes. Conclusions The present study suggests that CcIRF6 is involved in the antiviral and antibacterial immune response of common carp, and negatively regulate the expression of IFN and NF-κB signalling pathways, which provides a theoretical basis for the study and prevention of fish disease pathogenesis.https://doi.org/10.1186/s12917-022-03538-4Interferon regulatory factor 6 (IRF6)Poly(I:C)Aeromonas hydrophilaInterferonNF-κBCommon carp (Cyprinus carpio L.)
spellingShingle Yaxin Liang
Rongrong Liu
Jiahui Zhang
Yixin Chen
Shijuan Shan
Yaoyao Zhu
Guiwen Yang
Hua Li
Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
BMC Veterinary Research
Interferon regulatory factor 6 (IRF6)
Poly(I:C)
Aeromonas hydrophila
Interferon
NF-κB
Common carp (Cyprinus carpio L.)
title Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
title_full Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
title_fullStr Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
title_full_unstemmed Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
title_short Negative regulation of interferon regulatory factor 6 (IRF6) in interferon and NF-κB signalling pathways of common carp (Cyprinus carpio L.)
title_sort negative regulation of interferon regulatory factor 6 irf6 in interferon and nf κb signalling pathways of common carp cyprinus carpio l
topic Interferon regulatory factor 6 (IRF6)
Poly(I:C)
Aeromonas hydrophila
Interferon
NF-κB
Common carp (Cyprinus carpio L.)
url https://doi.org/10.1186/s12917-022-03538-4
work_keys_str_mv AT yaxinliang negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT rongrongliu negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT jiahuizhang negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT yixinchen negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT shijuanshan negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT yaoyaozhu negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT guiwenyang negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol
AT huali negativeregulationofinterferonregulatoryfactor6irf6ininterferonandnfkbsignallingpathwaysofcommoncarpcyprinuscarpiol