IRF-1 acts as a positive regulator in the transcription of grass carp (Ctenopharyngodon idella) IFN gene

Lai, Qinan; Lin, Gang; Ma, Meisheng; Huang, Shenghe; Li, Wen; Li, Dongming; Gu, Meihui; Mao, Huiling; Hu, Chengyu

doi:10.1016/j.fsi.2013.03.358

Cited by 25 publications

(9 citation statements)

References 37 publications

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“…Several studies indicated that fish IRF1 has the ability to activate the IFN promoter (22,23) and contributes to establishment of the host antiviral state (24,25). In the current study, we extend this notion by a line of evidence.…”

Section: Discussionsupporting

confidence: 73%

“…Recent studies showed that fish IRF3 and IRF7 are two master transcription factors essential for the RLR-triggered IFN signaling pathway, indicating conservation of function for vertebrate IRF family members (18)(19)(20)(21). Fish IRF1 displays an ability to activate the IFN promoter (22,23). Similarly, Japanese flounder Paralichthys olivaceus IRF1 contributes to establish an antiviral state in IRF1-overexpressing cells and modulates the early antiviral immune response in IRF1-vaccinated fish, likely by induction of IFN-like cytokines (24,25).…”

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confidence: 99%

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Zebrafish IRF1 Regulates IFN Antiviral Response through Binding to IFNϕ1 and IFNϕ3 Promoters Downstream of MyD88 Signaling

Feng

Zhang

et al. 2015

The Journal of Immunology

102

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In mammals, type I IFNs (mainly IFN-α/β) are primarily regulated by transcription factors of the IFN regulatory factor (IRF) family. Fish IFNs do not show a one-to-one orthologous relationship with mammalian type I IFN homologues. Using a bacterial one-hybrid reporter screening system and an overexpression approach to explore the molecular mechanism underlying fish IFN induction, we identified zebrafish Danio rerio IRF (DrIRF)1 as a positive regulator of the fish IFN antiviral response. Among 12 zebrafish IRF family genes, DrIRF1 is most abundant in zebrafish immune tissues, including head kidney and spleen; upon virus infection, it is one of most significantly induced genes. Overexpression of DrIRF1 induces the expression of IFN and IFN-stimulated genes, hence protecting epithelioma papulosum cyprini cells against spring viremia of carp virus infection. As a transcription factor with constitutively nuclear retention, DrIRF1 directly binds to the IFN-stimulated regulatory element/IRF-binding element sites of zebrafish IFN promoters, which are dependent on four conserved amino acids of the N-terminal DNA-binding domain helix α3 motif. Mutation of either residue reveals a differential requirement for DrIRF1-mediated activation of zebrafish IFNϕ1 and IFNϕ3 promoters. Notably, C-terminal phosphorylation of DrIRF1 is observed and is not required for in vitro binding of DrIRF1 to fish IFN promoters. Unlike DrIRF3 and DrIRF7, which are responsible for differential expression of zebrafish IFNϕ1 and IFNϕ3 through the retinoic acid–inducible gene I–like receptor pathway, DrIRF1 works in concert with MyD88 to activate zebrafish IFNϕ3 but not IFNϕ1. These results provide insights into the evolving function of IRF1 as a positive IFN regulator.

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Section: Discussionsupporting

confidence: 73%

mentioning

confidence: 99%

Zebrafish IRF1 Regulates IFN Antiviral Response through Binding to IFNϕ1 and IFNϕ3 Promoters Downstream of MyD88 Signaling

Feng

Zhang

et al. 2015

The Journal of Immunology

102

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“…In fish, 10 members of the IRF family have been identified and characterized (31)(32)(33)(34)(35)(36)(37). IRF10 is present in nonmammals including birds and fish (34,38,39).…”

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confidence: 99%

IFN Regulatory Factor 10 Is a Negative Regulator of the IFN Responses in Fish

Hong

et al. 2014

The Journal of Immunology

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IFN regulatory factor (IRF) 10 belongs to the IRF family and exists exclusively in birds and fish. Most IRFs have been identified as critical regulators in the IFN responses in both fish and mammals; however, the role of IRF10 is unclear. In this study, we identified IRF10 in zebrafish (Danio rerio) and found that it serves as a negative regulator to balance the innate antiviral immune responses. Zebrafish IRF10 (DrIRF10) was induced by intracellular polyinosinic:polycytidylic acid in ZF4 (zebrafish embryo fibroblast-like) cells. DrIRF10 inhibited the activation of zebrafish IFN1 (DrIFN1) and DrIFN3 promoters in epithelioma papulosum cyprinid cells in the presence or absence of polyinosinic:polycytidylic acid stimulation through direct interaction with the IFN promoters, and this inhibition was also shown to block IFN signaling. Overexpression of DrIRF10 was able to abolish the induction of DrIFN1 and DrIFN3 mediated by the retinoic acid–inducible gene I–like receptors. In addition, functional domain analysis of DrIRF10 showed that either the DNA binding domain or the IRF association domain is sufficient for its inhibitory activity for IFN signaling. Lastly, overexpression of DrIRF10 decreased the transcription level of several IFN-stimulated genes, resulting in the susceptibility of host cells to spring viremia of carp virus infection. Collectively, these data suggest that DrIRF10 inhibits the expression of DrIFN1 and DrIFN3 to avoid an excessive immune response, a unique regulation mechanism of the IFN responses in lower vertebrates.

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“…So far, IRF1 and IRF3 homologs have been cloned and indentified in some fish (Huang et al, 2010(Huang et al, , 2015Lai et al, 2013). Preliminary result indicated that IRF1 and IRF3 in fish share the same or similar function with the mammalia counterparts.…”

Section: Discussionmentioning

confidence: 99%

“…CiIRF-1, CiIRF1-nDBD and CiIRF-3, CiIRF3-nDBD were prepared as previously described (Lai et al, 2013). Three fragments of CiADAR1 promoter, namely the proximal region (CiADAR1Pp), the distal region (CiADAR1Pd) and the full sequence of CiADAR1 promoter (CiADAR1Pf), spanning from −367 to +22 bp, −1080 to −343 bp and −1080 to +22 bp relative to the transcription start site, were amplified with primer pairs CiADAR1PpF/CiADAR1PfR, CiADAR1PfF/CiADAR1PdR, and CiADAR1PfF/CiADAR1PfR (Supplementary Table S1), respectively.…”

Section: Gel Mobility Shift Assaysmentioning

confidence: 99%

Genome organization and transcriptional regulation of Adenosine Deaminase Acting on RNA gene 1 (ADAR1) in grass carp (Ctenopharyngodon idella)

Sun

Wang

Liu

et al. 2015

Developmental & Comparative Immunology

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IRF-1 acts as a positive regulator in the transcription of grass carp (Ctenopharyngodon idella) IFN gene

Cited by 25 publications

References 37 publications

Zebrafish IRF1 Regulates IFN Antiviral Response through Binding to IFNϕ1 and IFNϕ3 Promoters Downstream of MyD88 Signaling

Zebrafish IRF1 Regulates IFN Antiviral Response through Binding to IFNϕ1 and IFNϕ3 Promoters Downstream of MyD88 Signaling

IFN Regulatory Factor 10 Is a Negative Regulator of the IFN Responses in Fish

Genome organization and transcriptional regulation of Adenosine Deaminase Acting on RNA gene 1 (ADAR1) in grass carp (Ctenopharyngodon idella)

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