Abstract

BackgroundCommon carp (Cyprinus carpio L.), one of the most economically valuable commercial farming fish species in China, is often infected by a variety of viruses. As the first line of defence against microbial pathogens, the innate immune system plays a crucial role in teleost fish, which are lower vertebrates. Interferon (IFN) regulatory factor 5 (IRF5) is a key molecule in antiviral immunity that regulating the expression of IFN and other pro-inflammatory cytokines. It is necessary to gain more insight into the common carp IFN system and the function of fish IRF5 in the antiviral and antibacterial response.ResultsIn the present study, we characterized the cDNA and genomic sequence of the IRF5 gene in common carp, and analysed tissue distribution and expression profile of this gene in response to polyinosinic:polycytidylic acid (poly I:C) and lipopolysaccharides (LPS) treatment. The common carp IRF5 (ccIRF5) gene is 5790 bp in length and is composed of 9 exons and 8 introns. The open reading frame (ORF) of ccIRF5 is 1554 bp, and encodes 517 amino acid protein. The putative ccIRF5 protein shares identity (65.4–90.0 %) with other fish IRF5s and contains a DNA binding domain (DBD), a middle region (MR), an IRF-associated domain (IAD), a virus activated domain (VAD) and two nuclear localization signals (NLSs) similar to those found in vertebrate IRF5. Phylogenetic analysis clustered ccIRF5 into the IRF5 subfamily with other vertebrate IRF5 and IRF6 genes. Real-time PCR analysis revealed that ccIRF5 mRNA was expressed in all examined tissues of healthy carps, with high levels observed in the gills and the brain. After poly I:C challenge, expression levels of ccIRF5, tumour-necrosis factor α (ccTNFα) and two IFN stimulated genes [ISGs (ccISG5 and ccPKR)] were up-regulated in seven immune-related tissues (liver, spleen, head kidney, foregut, hindgut, skin and gills). Furthermore, all four genes were up-regulated in vitro upon poly I:C and LPS challenges.ConclusionsOur findings suggest that IRF5 might play an important role in regulating the antiviral and antibacterial response in fish. These results could provide a clue for preventing common carp infection by pathogenic microorganisms present in the aquatic environment.Electronic supplementary materialThe online version of this article (doi:10.1186/s12917-016-0750-4) contains supplementary material, which is available to authorized users.

Highlights

  • Common carp (Cyprinus carpio L.), one of the most economically valuable commercial farming fish species in China, is often infected by a variety of viruses

  • Eleven interferon regulatory factor (IRF) family members have been identified in vertebrate, including IRF1, IRF2, IRF3, IRF4 [ known as PU.1 interaction partner (PIP), lymphoidspecific IRF (LSIRF) or consensus sequence-binding protein in adult T-cell leukemia cell line or activated T cells (ICSAT)], IRF5, IRF6, IRF7, IRF8 [ known as IFN consensus sequence binding protein (ICSBP)], IRF9 [ called as interferon stimulated gene (ISG) factor 3 gamma (ISGF3γ)], IRF10 and IRF11

  • We reported the evolutionary relationship of common carp IRF5 gene with other IRF genes

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Summary

Introduction

Common carp (Cyprinus carpio L.), one of the most economically valuable commercial farming fish species in China, is often infected by a variety of viruses. Interferon (IFN) regulatory factor 5 (IRF5) is a key molecule in antiviral immunity that regulating the expression of IFN and other pro-inflammatory cytokines. Interferon (IFN) regulatory factors (IRFs) are key transcriptional mediators of virus-, bacteria- and IFNinduced signalling pathways, and they play an important role in antiviral defence, immune response, cell growth regulation, apoptosis and oncogenesis [1,2,3]. Eleven IRF family members have been identified in vertebrate, including IRF1, IRF2, IRF3, IRF4 [ known as PU. interaction partner (PIP), lymphoidspecific IRF (LSIRF) or consensus sequence-binding protein in adult T-cell leukemia cell line or activated T cells (ICSAT)], IRF5, IRF6, IRF7, IRF8 [ known as IFN consensus sequence binding protein (ICSBP)], IRF9 [ called as ISG factor 3 gamma (ISGF3γ)], IRF10 and IRF11. IRF-associated domain (IAD) in the C-terminal of IRF3-11 mediates the interactions between IRFs and other protein to form transcriptional complexes [7]

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