A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses
Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the em...
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| Published in | PLoS pathogens Vol. 13; no. 3; p. e1006258 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
09.03.2017
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1006258 |
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| Abstract | Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2-/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2-/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis. |
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| AbstractList | Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2-/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2-/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis. Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2.sup.-/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2.sup.-/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis. Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2-/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2-/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis.Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2-/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2-/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis. Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas, causing large human outbreaks associated with fetal abnormalities and neurological disease in adults. The factors that contributed to the emergence, spread and change in pathogenesis of ZIKV are not understood. We previously reported that ZIKV evades cellular antiviral responses by targeting STAT2 for degradation in human cells. In this study, we demonstrate that Stat2 -/- mice are highly susceptible to ZIKV infection, recapitulate virus spread to the central nervous system (CNS), gonads and other visceral organs, and display neurological symptoms. Further, we exploit this model to compare ZIKV pathogenesis caused by a panel of ZIKV strains of a range of spatiotemporal history of isolation and representing African and Asian lineages. We observed that African ZIKV strains induce short episodes of severe neurological symptoms followed by lethality. In comparison, Asian strains manifest prolonged signs of neuronal malfunctions, occasionally causing death of the Stat2 -/- mice. African ZIKV strains induced higher levels of inflammatory cytokines and markers associated with cellular infiltration in the infected brain in mice, which may explain exacerbated pathogenesis in comparison to those of the Asian lineage. Interestingly, viral RNA levels in different organs did not correlate with the pathogenicity of the different strains. Taken together, we have established a new murine model that supports ZIKV infection and demonstrate its utility in highlighting intrinsic differences in the inflammatory response induced by different ZIKV strains leading to severity of disease. This study paves the way for the future interrogation of strain-specific changes in the ZIKV genome and their contribution to viral pathogenesis. Zika virus is the most recent viral pathogen to cause a global public health emergency. It is distinct from other flaviviruses in its ability to cause transplacental infection, fetal abnormalities and vector independent transmission through body fluids in humans. Over the last year, there has been rapid progress in the development of animal models, which can be used to study ZIKV pathogenesis. In this study, we demonstrate for the first time that Stat2 -/- mice are highly susceptible to ZIKV infection and recapitulate aspects of ZIKV pathogenesis and disease. We use this model to delineate whether strain specific differences in ZIKV pathogenesis exist, using diverse strains representing both African and Asian lineages. We show that African strains in general are more virulent than Asian strains and their pathogenicity associates closely with the degree of inflammatory immune response in the CNS of infected mice, and does not necessarily correlate with viral RNA levels. Thus, we establish Stat2 -/- mice as new model to study ZIKV pathogenesis and use it to characterize inherent differences in the virulence among ZIKV strains. More importantly, we also highlight a potential role of the host inflammatory immune response in mediating differential pathogenesis among ZIKV strains. |
| Audience | Academic |
| Author | García-Sastre, Adolfo Albrecht, Randy A. Krammer, Florian Brown, Julia A. Evans, Matthew J. Balasubramaniam, Vinod R. M. T. Bardina, Susana V. Fernandez-Sesma, Ana Maringer, Kevin Grant, Alesha Tripathi, Shashank Schwarz, Megan C. Sourisseau, Marion Maestre, Ana M. Mena, Ignacio Lim, Jean K. |
| AuthorAffiliation | NIH, UNITED STATES 2 Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America 1 Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America 3 The Graduate School of Biological Sciences at the Icahn School of Medicine at Mount Sinai, Microbiology Training Area, New York, New York, United States of America 4 Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America |
| AuthorAffiliation_xml | – name: 3 The Graduate School of Biological Sciences at the Icahn School of Medicine at Mount Sinai, Microbiology Training Area, New York, New York, United States of America – name: 4 Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America – name: NIH, UNITED STATES – name: 2 Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America – name: 1 Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America |
| Author_xml | – sequence: 1 givenname: Shashank surname: Tripathi fullname: Tripathi, Shashank – sequence: 2 givenname: Vinod R. M. T. surname: Balasubramaniam fullname: Balasubramaniam, Vinod R. M. T. – sequence: 3 givenname: Julia A. orcidid: 0000-0002-9172-069X surname: Brown fullname: Brown, Julia A. – sequence: 4 givenname: Ignacio orcidid: 0000-0001-5464-7086 surname: Mena fullname: Mena, Ignacio – sequence: 5 givenname: Alesha surname: Grant fullname: Grant, Alesha – sequence: 6 givenname: Susana V. orcidid: 0000-0002-6776-2697 surname: Bardina fullname: Bardina, Susana V. – sequence: 7 givenname: Kevin orcidid: 0000-0003-0977-8807 surname: Maringer fullname: Maringer, Kevin – sequence: 8 givenname: Megan C. orcidid: 0000-0001-8715-2039 surname: Schwarz fullname: Schwarz, Megan C. – sequence: 9 givenname: Ana M. surname: Maestre fullname: Maestre, Ana M. – sequence: 10 givenname: Marion surname: Sourisseau fullname: Sourisseau, Marion – sequence: 11 givenname: Randy A. orcidid: 0000-0003-4008-503X surname: Albrecht fullname: Albrecht, Randy A. – sequence: 12 givenname: Florian surname: Krammer fullname: Krammer, Florian – sequence: 13 givenname: Matthew J. orcidid: 0000-0002-4991-3877 surname: Evans fullname: Evans, Matthew J. – sequence: 14 givenname: Ana surname: Fernandez-Sesma fullname: Fernandez-Sesma, Ana – sequence: 15 givenname: Jean K. surname: Lim fullname: Lim, Jean K. – sequence: 16 givenname: Adolfo orcidid: 0000-0002-6551-1827 surname: García-Sastre fullname: García-Sastre, Adolfo |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28278235$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-04181130$$DView record in HAL |
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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: Tripathi S, Balasubramaniam VRMT, Brown JA, Mena I, Grant A, Bardina SV, et al. (2017) A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses. PLoS Pathog 13(3): e1006258. https://doi.org/10.1371/journal.ppat.1006258 Distributed under a Creative Commons Attribution 4.0 International License 2017 Tripathi et al 2017 Tripathi 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: Tripathi S, Balasubramaniam VRMT, Brown JA, Mena I, Grant A, Bardina SV, et al. (2017) A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses. PLoS Pathog 13(3): e1006258. https://doi.org/10.1371/journal.ppat.1006258 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 PMCID: PMC5373643 Current address: University of Surrey, Surrey, United Kingdom Conceptualization: AGS ST FK.Data curation: ST VRMTB JAB IM.Formal analysis: ST JAB IM.Funding acquisition: AGS AFS.Investigation: ST VRMTB JAB IM RAA MCS.Methodology: ST IM.Project administration: ST AGS.Resources: AGS AFS JKL SVB MS KM AMM AG.Software: ST JAB.Supervision: AGS.Validation: ST.Visualization: ST IM.Writing – original draft: ST.Writing – review & editing: AGS JKL FK MJE IM. The authors have declared that no competing interests exist. |
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| Snippet | Zika virus (ZIKV) is a mosquito borne flavivirus, which was a neglected tropical pathogen until it emerged and spread across the Pacific Area and the Americas,... |
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| SubjectTerms | Abnormalities Analysis Animals Aquatic insects Biology and life sciences Central nervous system Cytokines Disease Disease Models, Animal Disease susceptibility Epidemics Flavivirus Global health Gonads Health aspects Host-virus relationships Immune response Infections Inflammation Inflammation - immunology Inflammation - virology Inflammatory response Interferon Interrogation Lethality Life Sciences Malfunctions Medicine Medicine and Health Sciences Mice Mice, Inbred C57BL Mice, Knockout Microbiology and Parasitology Neurological diseases Organs Outbreaks Pathogenesis Pathogens Phylogeny Real-Time Polymerase Chain Reaction Research and Analysis Methods Signs and symptoms Stem cells Vector-borne diseases Virology Viruses West Nile virus Zika Virus Zika Virus - genetics Zika Virus - immunology Zika Virus - pathogenicity Zika Virus Infection Zika Virus Infection - immunology |
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| Title | A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/28278235 https://www.proquest.com/docview/1900163047 https://www.proquest.com/docview/1876500491 https://hal.inrae.fr/hal-04181130 https://pubmed.ncbi.nlm.nih.gov/PMC5373643 https://doaj.org/article/219cc2204ce745298f85c5ac7cb53e57 http://dx.doi.org/10.1371/journal.ppat.1006258 |
| Volume | 13 |
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