The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses

Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral...

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Veröffentlicht in:PLoS neglected tropical diseases Jg. 11; H. 1; S. e0005272
Hauptverfasser: Dietrich, Isabelle, Shi, Xiaohong, McFarlane, Melanie, Watson, Mick, Blomström, Anne-Lie, Skelton, Jessica K., Kohl, Alain, Elliott, Richard M., Schnettler, Esther
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Public Library of Science 06.01.2017
Public Library of Science (PLoS)
Schlagworte:
Aedes - genetics
Aedes - immunology
Aedes - virology
Analysis
Animals
Aquatic insects
Biology and life sciences
Bunyaviruses
Ceratopogonidae - genetics
Ceratopogonidae - immunology
Ceratopogonidae - virology
Colleges & universities
Councils
Genomes
Infections
Medicine and Health Sciences
Mosquitoes
Orthobunyavirus - physiology
Proteins
Public health
Research and analysis methods
RNA Interference
RNA polymerase
RNA, Small Interfering - genetics
RNA, Small Interfering - immunology
Tropical diseases
Tropism
Virology
Virus-vector relationships
Viruses
Glasgow Scotland
Scotland
Edinburgh Scotland
United Kingdom > UK
ISSN:1935-2735, 1935-2727, 1935-2735
Online-Zugang:Volltext
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Abstract Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown. The genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions. These findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
AbstractList Background Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown. Methodology/Principal Findings The genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions. Conclusions/Significance These findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown. The genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions. These findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown. The genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions. These findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
BACKGROUNDVector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown.METHODOLOGY/PRINCIPAL FINDINGSThe genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions.CONCLUSIONS/SIGNIFICANCEThese findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
A number of orthobunyaviruses such as Oropouche virus, La Crosse virus and Schmallenberg virus are important global human or animal pathogens transmitted by arthropod vectors. Further understanding of the antiviral control mechanisms in arthropod vectors is key to developing novel prevention strategies based on preventing transmission. Antiviral small RNA pathways such as the exogenous siRNA and piRNA pathways have been shown to mediate antiviral activity against positive-strand RNA arboviruses, but information about their activities against negative-strand RNA arboviruses is critically lacking. Here we show that in Aedes aegypti-derived mosquito cells, the antiviral responses to mosquito-borne orthobunyaviruses is largely mediated by both siRNA and piRNA pathways, whereas the piRNA pathway plays only a minor role in controlling midge-borne orthobunyaviruses. This suggests that vector specificity is in part controlled by antiviral responses that depend on the host species. These findings contribute significantly to our understanding of arbovirus-vector interactions.
  Background Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus infections have been shown to induce the exogenous small interfering RNA (siRNA) and Piwi-interacting RNA (piRNA) pathways, but direct antiviral activity by these host responses in mosquito cells has only been demonstrated against a limited number of positive-strand RNA arboviruses. For bunyaviruses in general, the relative contribution of small RNA pathways in antiviral defences is unknown. Methodology/Principal Findings The genus Orthobunyavirus in the Bunyaviridae family harbours a diverse range of mosquito-, midge- and tick-borne arboviruses. We hypothesized that differences in the antiviral RNAi response in vector versus non-vector cells may exist and that could influence viral host range. Using Aedes aegypti-derived mosquito cells, mosquito-borne orthobunyaviruses and midge-borne orthobunyaviruses we showed that bunyavirus infection commonly induced the production of small RNAs and the effects of the small RNA pathways on individual viruses differ in specific vector-arbovirus interactions. Conclusions/Significance These findings have important implications for our understanding of antiviral RNAi pathways and orthobunyavirus-vector interactions and tropism.
Audience Academic
Author Dietrich, Isabelle
Schnettler, Esther
Kohl, Alain
Watson, Mick
Blomström, Anne-Lie
Skelton, Jessica K.
Elliott, Richard M.
Shi, Xiaohong
McFarlane, Melanie
AuthorAffiliation 2 Roslin Institute, Edinburgh, Scotland, United Kingdom
Tulane School of Public Health and Tropical Medicine, UNITED STATES
1 MRC-University of Glasgow Centre for Virus Research, Glasgow, Scotland, United Kingdom
AuthorAffiliation_xml – name: 2 Roslin Institute, Edinburgh, Scotland, United Kingdom
– name: 1 MRC-University of Glasgow Centre for Virus Research, Glasgow, Scotland, United Kingdom
– name: Tulane School of Public Health and Tropical Medicine, UNITED STATES
Author_xml – sequence: 1
  givenname: Isabelle
  surname: Dietrich
  fullname: Dietrich, Isabelle
– sequence: 2
  givenname: Xiaohong
  surname: Shi
  fullname: Shi, Xiaohong
– sequence: 3
  givenname: Melanie
  surname: McFarlane
  fullname: McFarlane, Melanie
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  givenname: Mick
  surname: Watson
  fullname: Watson, Mick
– sequence: 5
  givenname: Anne-Lie
  surname: Blomström
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  givenname: Alain
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  surname: Elliott
  fullname: Elliott, Richard M.
– sequence: 9
  givenname: Esther
  surname: Schnettler
  fullname: Schnettler, Esther
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28060823$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dietrich I, Shi X, McFarlane M, Watson M, Blomström A-L, Skelton JK, et al. (2017) The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses. PLoS Negl Trop Dis 11(1): e0005272. doi:10.1371/journal.pntd.0005272
2017 Dietrich et al 2017 Dietrich et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dietrich I, Shi X, McFarlane M, Watson M, Blomström A-L, Skelton JK, et al. (2017) The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses. PLoS Negl Trop Dis 11(1): e0005272. doi:10.1371/journal.pntd.0005272
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dietrich I, Shi X, McFarlane M, Watson M, Blomström A-L, Skelton JK, et al. (2017) The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses. PLoS Negl Trop Dis 11(1): e0005272. doi:10.1371/journal.pntd.0005272
– notice: 2017 Dietrich et al 2017 Dietrich et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dietrich I, Shi X, McFarlane M, Watson M, Blomström A-L, Skelton JK, et al. (2017) The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses. PLoS Negl Trop Dis 11(1): e0005272. doi:10.1371/journal.pntd.0005272
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Current address: Nuffield Department of Experimental Medicine, University of Oxford, Oxford, United Kingdom
Current address: BNITM, Hamburg, Germany
Current address: Section of Virology, Department of Medicine, Imperial College London, St Mary's Hospital, London, United Kingdom
Conceptualization: ID ES RME XS ALB AK.Data curation: MW ES AK.Formal analysis: ID MM MW ALB XS ES.Investigation: ID XS MM ALB JKS MW.Methodology: ID ES RME AK XS ALB MW.Project administration: ES AK.Resources: MW.Software: MW.Supervision: ES RME AK.Validation: ID XS JKS ALB MM.Visualization: ID XS ALB MM MW ES.Writing – original draft: ID AK ES.Writing – review & editing: ID XS MM MW ALB AK RME ES.
Current address: Section of Virology, Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, Uppsala, Sweden
The authors have declared that no competing interests exist.
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Snippet Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways. Arbovirus...
Background Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways....
BACKGROUNDVector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways....
A number of orthobunyaviruses such as Oropouche virus, La Crosse virus and Schmallenberg virus are important global human or animal pathogens transmitted by...
BackgroundVector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways....
  Background Vector arthropods control arbovirus replication and spread through antiviral innate immune responses including RNA interference (RNAi) pathways....
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SubjectTerms Aedes - genetics
Aedes - immunology
Aedes - virology
Analysis
Animals
Aquatic insects
Biology and life sciences
Bunyaviruses
Ceratopogonidae - genetics
Ceratopogonidae - immunology
Ceratopogonidae - virology
Colleges & universities
Councils
Genomes
Infections
Medicine and Health Sciences
Mosquitoes
Orthobunyavirus - physiology
Proteins
Public health
Research and analysis methods
RNA Interference
RNA polymerase
RNA, Small Interfering - genetics
RNA, Small Interfering - immunology
Tropical diseases
Tropism
Virology
Virus-vector relationships
Viruses
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Title The Antiviral RNAi Response in Vector and Non-vector Cells against Orthobunyaviruses
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Volume 11
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