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Interferon signaling in Peromyscus leucopus confers a potent and specific restriction to vector-borne flaviviruses
Journal article   Open access   Peer reviewed

Interferon signaling in Peromyscus leucopus confers a potent and specific restriction to vector-borne flaviviruses

Adaeze O Izuogu, Kristin L McNally, Stephen E Harris, Brian H Youseff, John B Presloid, Christopher Burlak, Jason Munshi-South, Sonja M Best and R Travis Taylor
PloS one, v 12(6), pp e0179781-e0179781
26 Jun 2017
PMID: 28650973
url
https://doi.org/10.1371/journal.pone.0179781View
Published, Version of Record (VoR) Open

Abstract

Animals Cells, Cultured Disease Models, Animal Encephalitis Viruses, Tick-Borne - genetics Encephalitis Viruses, Tick-Borne - immunology Encephalitis Viruses, Tick-Borne - pathogenicity Encephalitis, Tick-Borne - genetics Encephalitis, Tick-Borne - immunology Encephalitis, Tick-Borne - virology Host Specificity - genetics Host Specificity - immunology Host-Pathogen Interactions - genetics Host-Pathogen Interactions - immunology Humans Interferon Type I - antagonists & inhibitors Interferon Type I - immunology Mice Peromyscus - genetics Peromyscus - immunology Peromyscus - virology Receptor, Interferon alpha-beta - antagonists & inhibitors Receptor, Interferon alpha-beta - genetics Receptor, Interferon alpha-beta - immunology RNA, Small Interfering - genetics RNA, Viral - genetics Signal Transduction - genetics Signal Transduction - immunology STAT1 Transcription Factor - antagonists & inhibitors STAT1 Transcription Factor - genetics STAT1 Transcription Factor - immunology Viral Nonstructural Proteins - immunology Virus Replication - genetics Virus Replication - immunology
Tick-borne flaviviruses (TBFVs), including Powassan virus and tick-borne encephalitis virus cause encephalitis or hemorrhagic fevers in humans with case-fatality rates ranging from 1-30%. Despite severe disease in humans, TBFV infection of natural rodent hosts has little noticeable effect. Currently, the basis for resistance to disease is not known. We hypothesize that the coevolution of flaviviruses with their respective hosts has shaped the evolution of potent antiviral factors that suppress virus replication and protect the host from lethal infection. In the current study, we compared virus infection between reservoir host cells and related susceptible species. Infection of primary fibroblasts from the white-footed mouse (Peromyscus leucopus, a representative host) with a panel of vector-borne flaviviruses showed up to a 10,000-fold reduction in virus titer compared to control Mus musculus cells. Replication of vesicular stomatitis virus was equivalent in P. leucopus and M. musculus cells suggesting that restriction was flavivirus-specific. Step-wise comparison of the virus infection cycle revealed a significant block to viral RNA replication, but not virus entry, in P. leucopus cells. To understand the role of the type I interferon (IFN) response in virus restriction, we knocked down signal transducer and activator of transcription 1 (STAT1) or the type I IFN receptor (IFNAR1) by RNA interference. Loss of IFNAR1 or STAT1 significantly relieved the block in virus replication in P. leucopus cells. The major IFN antagonist encoded by TBFV, nonstructural protein 5, was functional in P. leucopus cells, thus ruling out ineffective viral antagonism of the host IFN response. Collectively, this work demonstrates that the IFN response of P. leucopus imparts a strong and virus-specific barrier to flavivirus replication. Future identification of the IFN-stimulated genes responsible for virus restriction specifically in P. leucopus will yield mechanistic insight into efficient control of virus replication and may inform the development of antiviral therapeutics.

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Collaboration types
Domestic collaboration
Web of Science research areas
Virology
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