miR-146a promotes Borna disease virus 1 replication through IRAK1/TRAF6/NF-κB signaling pathway.


Journal

Virus research
ISSN: 1872-7492
Titre abrégé: Virus Res
Pays: Netherlands
ID NLM: 8410979

Informations de publication

Date de publication:
02 10 2019
Historique:
received: 13 03 2019
revised: 19 06 2019
accepted: 17 07 2019
pubmed: 23 7 2019
medline: 1 7 2020
entrez: 23 7 2019
Statut: ppublish

Résumé

Borna disease virus 1 (BoDV-1) is a negative single-stranded RNA virus that is highly neurotropic. BoDV-1 infection can damage the central nervous system and cause inflammation. To survive in host cells, BoDV-1 must evade the host innate immune response. A previous study showed that miR-146a expression increased in neonatal rats infected with BoDV-1. miR-146a is a microRNA suggested to negatively regulate innate immune and inflammatory responses and antiviral pathways. Many groups have reported that its overexpression facilitates viral replication. However, it is unclear whether miR-146a is involved in escape from the host immune response during BoDV-1 infection. In this study, BoDV-1 was used to infect neonatal rats within 24 h of birth intracranially, as well as to infect human microglial cells (HMC3). miR-146a expression was analyzed by RT-qPCR. The TargetScanHuman database was used to find the target genes of miR-146a. A search of the binding sites of miR-146a and its target gene's 3'-untranslated region (3'UTR) was also performed using RNAhybrid software. The binding sites of miR-146a and the target gene's 3'UTR were detected by dual luciferase reporter assays. Overexpression and suppression studies of miR-146a were performed to determine its effect on BoDV-1 replication. The relative protein expression of members of the IRAK1/TRAF6/NF-κB signaling pathway was also evaluated by western blotting in HMC3. After BoDV-1 infection of neurons in vivo and of HMC3 cells, miR-146a expression was significantly upregulated. miR-146a overexpression in HMC3 cells promoted viral replication, while its inhibition inhibited it. Through the TargetScanHuman database, we identified the target genes of anti-inflammatory miR-146a: IRAK1 and TRAF6. We also found that BoDV-1 could inhibit IRAK1 and TRAF6 expression in HMC3 cells. Moreover, we showed that the inhibition of IRAK1 and TRAF6 also led to decreases in the expression of P65 and phosphorylated P65 in the downstream NF-κB pathway. Subsequently, we confirmed the interaction of miR-146a with IRAK1 and TRAF6 by luciferase assay. Our results suggest that miR-146a inhibits the IRAK1/TRAF6/NF-κB signaling pathway to facilitate BoDV-1 survival in host cells.

Sections du résumé

BACKGROUND/AIMS
Borna disease virus 1 (BoDV-1) is a negative single-stranded RNA virus that is highly neurotropic. BoDV-1 infection can damage the central nervous system and cause inflammation. To survive in host cells, BoDV-1 must evade the host innate immune response. A previous study showed that miR-146a expression increased in neonatal rats infected with BoDV-1. miR-146a is a microRNA suggested to negatively regulate innate immune and inflammatory responses and antiviral pathways. Many groups have reported that its overexpression facilitates viral replication. However, it is unclear whether miR-146a is involved in escape from the host immune response during BoDV-1 infection.
METHODS
In this study, BoDV-1 was used to infect neonatal rats within 24 h of birth intracranially, as well as to infect human microglial cells (HMC3). miR-146a expression was analyzed by RT-qPCR. The TargetScanHuman database was used to find the target genes of miR-146a. A search of the binding sites of miR-146a and its target gene's 3'-untranslated region (3'UTR) was also performed using RNAhybrid software. The binding sites of miR-146a and the target gene's 3'UTR were detected by dual luciferase reporter assays. Overexpression and suppression studies of miR-146a were performed to determine its effect on BoDV-1 replication. The relative protein expression of members of the IRAK1/TRAF6/NF-κB signaling pathway was also evaluated by western blotting in HMC3.
RESULTS
After BoDV-1 infection of neurons in vivo and of HMC3 cells, miR-146a expression was significantly upregulated. miR-146a overexpression in HMC3 cells promoted viral replication, while its inhibition inhibited it. Through the TargetScanHuman database, we identified the target genes of anti-inflammatory miR-146a: IRAK1 and TRAF6. We also found that BoDV-1 could inhibit IRAK1 and TRAF6 expression in HMC3 cells. Moreover, we showed that the inhibition of IRAK1 and TRAF6 also led to decreases in the expression of P65 and phosphorylated P65 in the downstream NF-κB pathway. Subsequently, we confirmed the interaction of miR-146a with IRAK1 and TRAF6 by luciferase assay.
CONCLUSION
Our results suggest that miR-146a inhibits the IRAK1/TRAF6/NF-κB signaling pathway to facilitate BoDV-1 survival in host cells.

Identifiants

pubmed: 31330207
pii: S0168-1702(19)30176-5
doi: 10.1016/j.virusres.2019.197671
pii:
doi:

Substances chimiques

3' Untranslated Regions 0
NF-kappa B 0
TNF Receptor-Associated Factor 6 0
IRAK1 protein, rat EC 2.7.11.1
Interleukin-1 Receptor-Associated Kinases EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

197671

Informations de copyright

Copyright © 2019 Elsevier B.V. All rights reserved.

Auteurs

Xiong Zhang (X)

Department of Neurology, The First Affiliated Hospital, Chongqing Medical University, Chongqing, China; Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Yujie Guo (Y)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Xiaoyan Xu (X)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Tian Tang (T)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Lin Sun (L)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China; Department of Pain, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China.

Haiyang Wang (H)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Wei Zhou (W)

Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China.

Liang Fang (L)

Department of Neurology, Yongchuan Hospital, Chongqing Medical University, Chongqing, China.

Qi Li (Q)

Department of Neurology, The First Affiliated Hospital, Chongqing Medical University, Chongqing, China.

Peng Xie (P)

Department of Neurology, The First Affiliated Hospital, Chongqing Medical University, Chongqing, China; Chongqing Key Laboratory of Neurobiology, Chongqing Medical University, Chongqing, China; Department of Neurology, Yongchuan Hospital, Chongqing Medical University, Chongqing, China. Electronic address: xiepeng@cqmu.edu.cn.

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Classifications MeSH