A cytosolic sensor, PmDDX41, mediates antiviral immune response in black tiger shrimp Penaeus monodon

Soponpong, Suthinee; Amparyup, Piti; Tassanakajon, Anchalee

doi:10.1016/j.dci.2017.12.013

Cited by 17 publications

(18 citation statements)

References 44 publications

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“…In a previous study, we showed that white spot syndrome virus (WSSV) (a double-stranded DNA virus) and yellow head virus (YHV) (a single-stranded RNA virus) could induce the expression of PmDDX41 (17). Here, we injected the nucleic acid mimics, poly(dA:dT) and poly(I:C), and used qRT-PCR to investigate the effect of these injections on Pm DDX41 gene expression in shrimp hemocytes.…”

Section: Resultsmentioning

confidence: 99%

“…DDX41 has been reported to be highly conserved across a number of different species (17). We chose to use HEK 293T cells to further investigate the mechanism by which Pm DDX41 can sense nucleic acids.…”

Section: Resultsmentioning

confidence: 99%

“…DDX41 has also been identified in the black tiger shrimp Penaeus monodon ( Pm DDX41); the expression of Pm DDX41 was up-regulated in response to white spot syndrome virus (WSSV), a DNA virus with severe pathogenic effects on shrimp populations. Silencing the Pm DDX41 gene resulted in the rapid death of WSSV-infected shrimp and a reduction in the expression levels of several immune genes related to immune signaling pathways and antimicrobial peptides (17). In this study, we further characterized the function of Pm DDX41 as a nucleic acid sensor in shrimp and investigated how this sensor interacts with dsDNA and STING to send signals that ultimately activated innate immune responses in a human embryonic kidney cell line (HEK293T).…”

Section: Introductionmentioning

confidence: 99%

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A Cytosolic Sensor, PmDDX41, Binds Double Stranded-DNA and Triggers the Activation of an Innate Antiviral Response in the Shrimp Penaeus monodon via the STING-Dependent Signaling Pathway

et al. 2019

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Helicase DDX41 is a cytosolic sensor capable of detecting double-stranded DNA in mammals. However, the function of DDX41 remains poorly understood in invertebrates. In a previous study, we identified the first DDX41 sensor in the black tiger shrimp Penaeus monodon (PmDDX41) and showed that it played a role in anti-viral response. In the present study, we demonstrated that PmDDX41 was localized in the cytoplasm of shrimp hemocytes. However, PmDDX41 was localized in both the cytoplasm and nucleus of hemocytes in the presence of white spot syndrome virus (WSSV) infection or when stimulated by the nucleic acid mimics, poly(dA:dT) and poly(I:C). Similar results were observed when PmDDX41 was transfected into human embryonic kidney 293T (HEK293T) cells. Immunoprecipitation further demonstrated that PmDDX41 bound to biotin-labeled poly(dA:dT) but not poly(I:C). The overexpression of shrimp PmDDX41 and mouse stimulator of interferon gene (MmSTING) in HEK293T cells synergistically promoted IFN-β and NF-κB promoter activity via the DEADc domain. Co-immunoprecipitation (Co-IP) also confirmed that there was an interaction between PmDDX41 and STING after stimulation with poly(dA:dT) but not poly(I:C). Our study is the first to demonstrate that PmDDX41 acts as a cytosolic DNA sensor that interacts with STING via its DEADc domain to trigger the IFN-β and NF-κB signaling pathways, thus activating antiviral innate immune responses.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Cytosolic Sensor, PmDDX41, Binds Double Stranded-DNA and Triggers the Activation of an Innate Antiviral Response in the Shrimp Penaeus monodon via the STING-Dependent Signaling Pathway

et al. 2019

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“…More recently, IKK from P. monodon including PmIKK β and PmIKK ε transcripts were suppressed when a DNA sensing molecule called DEAD (Asp-Glu-Ala-Asp)-box polypeptide 41 ( PmDDX41 ) was suppressed (37). The DDX41 is identified as a dsDNA-sensing receptor in mouse dendritic cells and involved in type I interferon regulation via interferon regulatory factors (IRF3 and IRF7) (38).…”

Section: Discussionmentioning

confidence: 99%

“…The DDX41 is identified as a dsDNA-sensing receptor in mouse dendritic cells and involved in type I interferon regulation via interferon regulatory factors (IRF3 and IRF7) (38). The silencing of PmDDX41 affects several downstream immune genes including transcription factors and AMPs (37). These results demonstrate the signaling cascade generated from the Pm DDX41 as a sensing molecule through Pm IKKβ and Pm IKKε for shrimp immune response.…”

Section: Discussionmentioning

confidence: 99%

Penaeus monodon IKKs Participate in Regulation of Cytokine-Like System and Antiviral Responses of Innate Immune System

et al. 2019

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The IKK-NF-κB signaling cascade is one of the crucial responsive mechanisms in inflammatory and immune responses. The key kinase proteins called inhibitor of kappa B kinases (IKKs) serve as the core elements involved in cascade activation. Here, the complete ORFs of IKK homologs, PmIKK β , PmIKK ε 1 , and PmIKK ε 2 , from the black tiger shrimp Penaeus monodon were identified and characterized for their functions in shrimp antiviral responses. The PmIKK transcripts were widely expressed in various examined tissues and the Pm IKKε protein was detected in all three types of shrimp hemocytes. Only the PmIKK ε 1 and PmIKK ε 2 were responsive to white spot syndrome virus (WSSV), yellow head virus (YHV) and a bacterium Vibrio harveyi infection, while the PmIKK β exhibited no significant response to pathogen infection. On the contrary, suppression of PmIKK β and PmIKK ε by dsRNA-mediated RNA interference (RNAi) resulted in a rapid death of WSSV-infected shrimp and the significant reduction of an IFN-like PmVago4 transcript. Whereas, the mRNA levels of the antimicrobial peptides, ALFPm3 and CrustinPm5 , and a transcription factor, PmDorsal were significantly increased, those of ALFPm6, CrustinPm1, CrustinPm7, PmVago1, PmRelish , and PmCactus were unaffected. Overexpression of Pm IKKβ and Pm IKKε in HEK293T cells differentially activated the NF-κB and IFNβ promoter activities, respectively. These results suggest that the Pm IKKβ and Pm IKKε may act as common factors regulating the expression of immune-related genes from various signaling pathways. Interestingly, the Pm IKKs may also contribute a possible role in shrimp cytokine-like system and cross-talking between signaling transductions in innate immune responses.

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Nucleic Acid Sensing in Invertebrate Antiviral Immunity

Wang

2019

International Review of Cell and Molecular Biology

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A cytosolic sensor, PmDDX41, mediates antiviral immune response in black tiger shrimp Penaeus monodon

Cited by 17 publications

References 44 publications

A Cytosolic Sensor, PmDDX41, Binds Double Stranded-DNA and Triggers the Activation of an Innate Antiviral Response in the Shrimp Penaeus monodon via the STING-Dependent Signaling Pathway

A Cytosolic Sensor, PmDDX41, Binds Double Stranded-DNA and Triggers the Activation of an Innate Antiviral Response in the Shrimp Penaeus monodon via the STING-Dependent Signaling Pathway

Penaeus monodon IKKs Participate in Regulation of Cytokine-Like System and Antiviral Responses of Innate Immune System

Nucleic Acid Sensing in Invertebrate Antiviral Immunity

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