NOD2 in zebrafish functions in antibacterial and also antiviral responses via NF-κB, and also MDA5, RIG-I and MAVS

Zou, Peng; Chang, Ming Xian; Liu, Ying; Xue, Na; Li, Jun Hua; Chen, Shan Nan; Nie, Pin

doi:10.1016/j.fsi.2016.05.031

Cited by 59 publications

(44 citation statements)

References 59 publications

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“…Dr RIG-I could negatively regulate MDP-initiated NOD2 signaling, and Dr NOD2 could negatively regulate LMW poly I:C initiated RIG-I signaling. NOD2 was recently confirmed to interact with RIG-I in a zebrafish cell line (ZF4) by co-immunoprecipitation analysis [38], and we established that this interaction relies on the CARD domain in HEK293T cells (Figure S1). Moreover, the interaction of mammalian NOD2 with RIG-I and mutual regulation have been observed in human cell lines [39].…”

Section: Discussionsupporting

confidence: 60%

“…Extensive related studies have been conducted using zebrafish, and the results indicated that Dr NOD2 and Dr RIG-I were highly conserved and similar to their mammalian counterparts [36,37,38]. Thus, the zebrafish is an attractive model organism to investigate the functional relevance and mutual regulation between RIG-I and NOD2 signaling pathways not only for teleosts, but also for higher species.…”

Section: Introductionmentioning

confidence: 99%

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Mutual Regulation of NOD2 and RIG-I in Zebrafish Provides Insights into the Coordination between Innate Antibacterial and Antiviral Signaling Pathways

Nie

Xiang

et al. 2017

IJMS

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Nucleotide-binding oligomerization domain-containing protein 2 (NOD2) and retinoic acid-inducible gene I (RIG-I) are two important cytosolic pattern recognition receptors (PRRs) in the recognition of pathogen-associated molecular patterns (PAMPs), initiating innate antibacterial and antiviral signaling pathways. However, the relationship between these PRRs, especially in teleost fish models, is rarely reported. In this article, we describe the mutual regulation of zebrafish NOD2 (DrNOD2) and RIG-I (DrRIG-I) in innate immune responses. Luciferase assays were conducted to determine the activation of NF-κB and interferon signaling. Morpholino-mediated knockdown and mRNA-mediated rescue were performed to further confirm the regulatory roles between DrNOD2 and DrRIG-I. Results showed that DrNOD2 and DrRIG-I shared conserved structural hallmarks with their mammalian counterparts, and activated DrRIG-I signaling can induce DrNOD2 production. Surprisingly, DrNOD2-initiated signaling can also induce DrRIG-I expression, indicating that a mutual regulatory mechanism may exist between them. Studies conducted using HEK293T cells and zebrafish embryos showed that DrRIG-I could negatively regulate DrNOD2-activated NF-κB signaling, and DrNOD2 could inhibit DrRIG-I-induced IFN signaling. Moreover, knocking down DrRIG-I expression by morpholino could enhance DrNOD2-initiated NF-κB activation, and vice versa, which could be rescued by their corresponding mRNAs. Results revealed a mutual feedback regulatory mechanism underlying NOD2 and RIG-I signaling pathways in teleosts. This mechanism reflects the coordination between cytosolic antibacterial and antiviral PRRs in the complex network of innate immunity.

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Section: Discussionsupporting

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Mutual Regulation of NOD2 and RIG-I in Zebrafish Provides Insights into the Coordination between Innate Antibacterial and Antiviral Signaling Pathways

Nie

Xiang

et al. 2017

IJMS

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“…However, NLR‐X1 expression was not induced by exposure to Poly(I:C), indicating that in goldfish ( Carassius auratus L.) , Poly(I:C) is not a ligand for NLR‐X1 (Xie et al., ). Zebrafish ( Danio rerio ) NOD2 showed a marked response to MDP stimulation, but was not responsive to stimulation with Poly(I:C), PGN, lipoteichoic acid (LTA), LPS, mannan, glucan or β‐1,3‐glucan; these findings indicate that zebrafish ( Danio rerio ) NOD2 may be a receptor for MDP (Zou et al., ), which is consistent with Nile tilapia ( Oreochromis niloticus ) (Gao et al., ). In Asian seabass ( Lates calcarifer ), NLR‐C3 responds to LPS, Poly(I:C) and PGN stimulation, indicating that these molecules are potential ligands of NLR‐C3 (Paria et al., ).…”

Section: Ligand Recognition By Nlrs In Teleost Fishmentioning

confidence: 56%

“…The role of NOD1 and NOD2 in bacterial and viral immune responses has been studied in mammals (Barnich, Aguirre, Reinecker, Xavier, & Podolsky, ; Kufer, Kremmer, Banks, & Philpott, ; Tattoli, Travassos, Carneiro, Magalhaes, & Girardin, ; Uehara et al., ), rohu ( Labeo rohita ) (Swain, Basu, Sahoo et al., ; Swain, Basu, Samanta et al., ), mrigal ( Cirrhinus mrigala ) (Swain, Basu, & Samanta, ), orange‐spotted grouper ( Epinephelus coioides ) (Hou et al., ), rainbow trout ( Oncorhynchus mykiss ) (Chang et al., ), grass carp ( Ctenopharyngodon idella ) (Chen et al., ), channel catfish ( Ictalurus punctatus ) (Sha et al., ) and zebrafish ( Danio rerio ) (Zou et al., ). In mammals, NOD1 and NOD2 can directly interact with IPS‐1 (interferon‐β promoter stimulator protein 1), resulting in the activation of NF‐κB (nuclear factor kappa B) and IRF‐3 (interferon regulatory factor 3).…”

Section: Antibacterial and Antiviral Functions Of Nlrs In Teleost Fishmentioning

confidence: 99%

Nucleotide‐binding and oligomerization domain (NOD)‐like receptors in teleost fish: Current knowledge and future perspectives

Zhang

Gao

et al. 2018

Journal of Fish Diseases

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Nucleotide-binding and oligomerization domain (NOD)-like receptors (NLRs) are a group of intracellular pathogen recognition receptors (PRRs) that play key roles in pathogen recognition and subsequent activation of innate immune signalling pathways. Expressions of several NLR subfamily members, including NOD1, NOD2, NLR-C3, NLR-C5 and NLR-X1 have been reported in many different teleost fish species. These receptors are activated by a variety of ligands, including lipopolysaccharides (LPS), peptidoglycans (PGN) and polyinosinic-polycytidylic acid [Poly(I:C)]. Synthetic dsRNA and bacterial or viral infections are known to stimulate these receptors both in vitro and in vivo. In this review, we focus on the identification, expression and function of teleost NLRs in response to bacterial or viral pathogens. Additionally, NLR ligand specificity and signalling pathways involved in the recognition of bacterial or viral stimuli are also summarized. This review focuses on current knowledge in this area and provides future perspectives regarding topics in need of additional investigation. Understanding the response of innate immune system to bacterial or viral infections in diverse species could inform the development of more effective therapies and vaccines.

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“…; Zou et al . ). The RLR family constitutes a family of soluble RNA helicases present in the cytosol.…”

Section: Introductionmentioning

confidence: 97%

Molecular cloning of MDA5, phylogenetic analysis of RIG‐I‐like receptors (RLRs) and differential gene expression of RLRs, interferons and proinflammatory cytokines after in vitro challenge with IPNV, ISAV and SAV in the salmonid cell line TO

Nerbøvik

Solheim

Eggestøl

et al. 2017

Journal of Fish Diseases

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The RIG-I receptors RIG-I, MDA5 and LGP2 are involved in viral recognition, and they have different ligand specificity and recognize different viruses. Activation of RIG-I-like receptors (RLRs) leads to production of cytokines essential for antiviral immunity. In fish, most research has focused on interferons, and less is known about the production of proinflammatory cytokines during viral infections. In this study, we have cloned the full-length MDA5 sequence in Atlantic salmon, and compared it with RIG-I and LGP2. Further, the salmonid cell line TO was infected with three fish pathogenic viruses, infectious pancreatic necrosis virus (IPNV), infectious salmon anaemia virus (ISAV) and salmonid alphavirus (SAV), and differential gene expression (DEG) analyses of RLRs, interferons (IFNa-d) and proinflammatory cytokines (TNF-α1, TNF-α2, IL-1β, IL-6, IL-12 p40s) were performed. The DEG analyses showed that the responses of proinflammatory cytokines in TO cells infected with IPNV and ISAV were profoundly different from SAV-infected cells. In the two aforementioned, TNF-α1 and TNF-α2 were highly upregulated, while in SAV-infected cells these cytokines were downregulated. Knowledge of virus recognition by the host and the immune responses during infection may help elucidate why and how some viruses can escape the immune system. Such knowledge is useful for the development of immune prophylactic measures.

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NOD2 in zebrafish functions in antibacterial and also antiviral responses via NF-κB, and also MDA5, RIG-I and MAVS

Cited by 59 publications

References 59 publications

Mutual Regulation of NOD2 and RIG-I in Zebrafish Provides Insights into the Coordination between Innate Antibacterial and Antiviral Signaling Pathways

Mutual Regulation of NOD2 and RIG-I in Zebrafish Provides Insights into the Coordination between Innate Antibacterial and Antiviral Signaling Pathways

Nucleotide‐binding and oligomerization domain (NOD)‐like receptors in teleost fish: Current knowledge and future perspectives

Molecular cloning of MDA5, phylogenetic analysis of RIG‐I‐like receptors (RLRs) and differential gene expression of RLRs, interferons and proinflammatory cytokines after in vitro challenge with IPNV, ISAV and SAV in the salmonid cell line TO

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