Identification of an IRF10 gene in common carp (Cyprinus carpio L.) and analysis of its function in the antiviral and antibacterial immune response

Yaoyao Zhu,Rongrong Liu,Huaping Zhao,Guiwen Yang,Hui Wang,Shijuan Shan,Xinping Chen,Hua Li

doi:10.1186/s12917-020-02674-z

Abstract

BackgroundInterferon (IFN) regulatory factors (IRFs), as transcriptional regulatory factors, play important roles in regulating the expression of type I IFN and IFN- stimulated genes (ISGs) in innate immune responses. In addition, they participate in cell growth and development and regulate oncogenesis.ResultsIn the present study, the cDNA sequence of IRF10 in common carp (Cyprinus carpio L.) was characterized (abbreviation, CcIRF10). The predicted protein sequence of CcIRF10 shared 52.7–89.2% identity with other teleost IRF10s and contained a DNA-binding domain (DBD), a nuclear localization signal (NLS) and an IRF-associated domain (IAD). Phylogenetic analysis showed that CcIRF10 had the closest relationship with IRF10 of Ctenopharyngodon idella. CcIRF10 transcripts were detectable in all examined tissues, with the highest expression in the gonad and the lowest expression in the head kidney. CcIRF10 expression was upregulated in the spleen, head kidney, foregut and hindgut upon polyinosinic:polycytidylic acid (poly I:C) and Aeromonas hydrophila stimulation and induced by poly I:C, lipopolysaccharide (LPS) and peptidoglycan (PGN) in peripheral blood leucocytes (PBLs) and head kidney leukocytes (HKLs) of C. carpio. In addition, overexpression of CcIRF10 was able to decrease the expression of the IFN and IFN-stimulated genes PKR and ISG15.ConclusionsThese results indicate that CcIRF10 participates in antiviral and antibacterial immunity and negatively regulates the IFN response, which provides new insights into the IFN system of C. carpio.

Highlights

Interferon (IFN) regulatory factors (IRFs), as transcriptional regulatory factors, play important roles in regulating the expression of type I IFN and IFN- stimulated genes (ISGs) in innate immune responses
Results cDNA cloning and molecular characterization of CcIRF10 The full-length cDNA of CcIRF10 was found to consist of 1274 bp
The results showed that the gene expression of IFN, PKR and ISG15 was reduced in the cells transfected with pcDNA3.1EGFP-CcIRF10, which were 83, 0.87 and 0.69% of the expression in control cells, respectively (P < 0.05, Fig. 6a-c)

Summary

Introduction

Interferon (IFN) regulatory factors (IRFs), as transcriptional regulatory factors, play important roles in regulating the expression of type I IFN and IFN- stimulated genes (ISGs) in innate immune responses. They participate in cell growth and development and regulate oncogenesis. Interferon (IFN) regulatory factors (IRFs), as transcriptional regulatory factors, play multiple important roles in host immune responses and other physiological processes; for example, they regulate the expression of type I IFN and IFNstimulated genes (ISGs) [1], the activation and differentiation of distinct immune cell populations, cell growth, differentiation and apoptosis [2, 3]. The N-terminal regions of IRFs share a highly conserved DNA-binding domain (DBD), which contains five or six tryptophan repeats [4]. Functional characterization of fish IRF10 has begun recently, and this gene has been identified in teleosts including zebrafish (Danio rerio) [9], orange spotted grouper (Epinephelus coioides) [10, 11], Japanese flounder (Paralichthys olivaceus) [12], Atlantic cod (Gadus morhua) [13, 14], grass carp (Ctenopharyngodon idella) [15], rainbow trout (Oncorhynchus mykiss) [15, 16], Asian swamp eel (Monopterus albus) [15, 17], mandarin fish (Siniperca chuatsi) [18], Senegalese sole (Solea senegalensis) [19] and blunt snout bream (Megalobrama amblycephala) [20]

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Discussion

Conclusion