Defining the range of pathogens susceptible to Ifitm3 restriction using a knockout mouse model

The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress through the late endosomal pathway. Further, single nucleotide polymorphisms (SNPs) in its sequence have been linked with risk of developing...

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Published inPloS one Vol. 8; no. 11; p. e80723
Main Authors Everitt, Aaron R, Clare, Simon, McDonald, Jacqueline U, Kane, Leanne, Harcourt, Katherine, Ahras, Malika, Lall, Amar, Hale, Christine, Rodgers, Angela, Young, Douglas B, Haque, Ashraful, Billker, Oliver, Tregoning, John S, Dougan, Gordon, Kellam, Paul
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 21.11.2013
Public Library of Science (PLoS)
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Abstract The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress through the late endosomal pathway. Further, single nucleotide polymorphisms (SNPs) in its sequence have been linked with risk of developing severe influenza virus infections in humans. The number of viruses restricted by this host protein has continued to grow since it was first demonstrated as playing an antiviral role; all of which enter cells via the endosomal pathway. We therefore sought to test the limits of antimicrobial restriction by Ifitm3 using a knockout mouse model. We showed that Ifitm3 does not impact on the restriction or pathogenesis of bacterial (Salmonella typhimurium, Citrobacter rodentium, Mycobacterium tuberculosis) or protozoan (Plasmodium berghei) pathogens, despite in vitro evidence. However, Ifitm3 is capable of restricting respiratory syncytial virus (RSV) in vivo either through directly restricting RSV cell infection, or by exerting a previously uncharacterised function controlling disease pathogenesis. This represents the first demonstration of a virus that enters directly through the plasma membrane, without the need for the endosomal pathway, being restricted by the IFITM family; therefore further defining the role of these antiviral proteins.
AbstractList The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress through the late endosomal pathway. Further, single nucleotide polymorphisms (SNPs) in its sequence have been linked with risk of developing severe influenza virus infections in humans. The number of viruses restricted by this host protein has continued to grow since it was first demonstrated as playing an antiviral role; all of which enter cells via the endosomal pathway. We therefore sought to test the limits of antimicrobial restriction by Ifitm3 using a knockout mouse model. We showed that Ifitm3 does not impact on the restriction or pathogenesis of bacterial (Salmonella typhimurium, Citrobacter rodentium, Mycobacterium tuberculosis) or protozoan (Plasmodium berghei) pathogens, despite in vitro evidence. However, Ifitm3 is capable of restricting respiratory syncytial virus (RSV) in vivo either through directly restricting RSV cell infection, or by exerting a previously uncharacterised function controlling disease pathogenesis. This represents the first demonstration of a virus that enters directly through the plasma membrane, without the need for the endosomal pathway, being restricted by the IFITM family; therefore further defining the role of these antiviral proteins.
The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress through the late endosomal pathway. Further, single nucleotide polymorphisms (SNPs) in its sequence have been linked with risk of developing severe influenza virus infections in humans. The number of viruses restricted by this host protein has continued to grow since it was first demonstrated as playing an antiviral role; all of which enter cells via the endosomal pathway. We therefore sought to test the limits of antimicrobial restriction by Ifitm3 using a knockout mouse model. We showed that Ifitm3 does not impact on the restriction or pathogenesis of bacterial ( Salmonella typhimurium, Citrobacter rodentium , Mycobacterium tuberculosis ) or protozoan ( Plasmodium berghei ) pathogens, despite in vitro evidence. However, Ifitm3 is capable of restricting respiratory syncytial virus (RSV) in vivo either through directly restricting RSV cell infection, or by exerting a previously uncharacterised function controlling disease pathogenesis. This represents the first demonstration of a virus that enters directly through the plasma membrane, without the need for the endosomal pathway, being restricted by the IFITM family; therefore further defining the role of these antiviral proteins.
Audience Academic
Author Harcourt, Katherine
Tregoning, John S
Billker, Oliver
Haque, Ashraful
Hale, Christine
Dougan, Gordon
Rodgers, Angela
Young, Douglas B
Everitt, Aaron R
McDonald, Jacqueline U
Kane, Leanne
Lall, Amar
Kellam, Paul
Clare, Simon
Ahras, Malika
AuthorAffiliation 4 Medical Research Council National Institute for Medical Research, London, United Kingdom
3 The Jenner Institute, University of Oxford, Oxford, United Kingdom
5 Malaria Immunology Laboratory, Queensland Institute of Medical Research and The Australian Centre for Vaccine Development, Herston, Brisbane, Queensland, Australia
6 Department of Infection, University College London, London, United Kingdom
Mayo Clinic, United States of America
1 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, United Kingdom
2 Mucosal Infection and Immunity Group, Section of Infectious Diseases, Department of Medicine, Imperial College London, London, United Kingdom
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24278312$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Everitt et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/3.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2013 Everitt et al 2013 Everitt et al
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: 2013 Everitt et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/3.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Conceived and designed the experiments: ARE SC AH DBY OB JST GD PK. Performed the experiments: ARE SC JUM LK KH MA AL CH AR DBY AH JST. Analyzed the data: ARE OB JST. Contributed reagents/materials/analysis tools: ARE SC JUM CH DBY AH OB JST GD PK. Wrote the manuscript: ARE SC OB JST PK.
Competing Interests: The authors have declared that no competing interests exist.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3836756/
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Snippet The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress...
The interferon-inducible transmembrane (IFITM) family of proteins has been shown to restrict a broad range of viruses in vitro and in vivo by halting progress...
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SubjectTerms Animal
Animals
Antiviral activity
Bacteria
Bacteria - metabolism
Biological response modifiers
Citrobacter
Citrobacter rodentium - growth & development
Citrobacter rodentium - physiology
Citrobacter rodentium/growth & development/physiology
College campuses
Disease control
Ethics
Gene expression
Genetic aspects
Genomes
Health aspects
Homeostasis
Immunology
In vivo methods and tests
Inbred C57BL
Infection
Infections
Infectious diseases
Influenza
Influenza viruses
Interferon
Kinetics
Knockout
Laboratories
Malaria - parasitology
Medical research
Membrane Proteins - deficiency
Membrane Proteins - metabolism
Membrane Proteins/deficiency/metabolism
Mice
Mice, Inbred C57BL
Mice, Knockout
Models, Animal
Mycobacterium tuberculosis - growth & development
Mycobacterium tuberculosis - physiology
Mycobacterium tuberculosis/growth & development/physiology
Pathogenesis
Pathogenic microorganisms
Pathogens
Phenotype
Plasmodium berghei
Plasmodium berghei - growth & development
Plasmodium berghei - physiology
Plasmodium berghei/growth & development/physiology
Proteins
Protozoa
Respiratory syncytial virus
Respiratory Syncytial Viruses - growth & development
Respiratory Syncytial Viruses - physiology
Respiratory Syncytial Viruses/growth & development/physiology
Salmonella
Salmonella typhimurium - physiology
Single nucleotide polymorphisms
Single-nucleotide polymorphism
Tuberculosis
Viral infections
Virology
Viruses
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Title Defining the range of pathogens susceptible to Ifitm3 restriction using a knockout mouse model
URI https://www.ncbi.nlm.nih.gov/pubmed/24278312
https://www.proquest.com/docview/1460504766
https://search.proquest.com/docview/1462190241
https://pubmed.ncbi.nlm.nih.gov/PMC3836756
https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-165861
https://doaj.org/article/9e3566d8772d4f319075c3ea2baea247
http://dx.doi.org/10.1371/journal.pone.0080723
Volume 8
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