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Bacteria and bacterial envelope components enhance mammalian reovirus thermostability

Enteric viruses encounter diverse environments as they migrate through the gastrointestinal tract to infect their hosts. The interaction of eukaryotic viruses with members of the host microbiota can greatly impact various aspects of virus biology, including the efficiency with which viruses can infe...

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Autores principales: Berger, Angela K., Yi, Hong, Kearns, Daniel B., Mainou, Bernardo A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5734793/
https://www.ncbi.nlm.nih.gov/pubmed/29211815
http://dx.doi.org/10.1371/journal.ppat.1006768
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author Berger, Angela K.
Yi, Hong
Kearns, Daniel B.
Mainou, Bernardo A.
author_facet Berger, Angela K.
Yi, Hong
Kearns, Daniel B.
Mainou, Bernardo A.
author_sort Berger, Angela K.
collection PubMed
description Enteric viruses encounter diverse environments as they migrate through the gastrointestinal tract to infect their hosts. The interaction of eukaryotic viruses with members of the host microbiota can greatly impact various aspects of virus biology, including the efficiency with which viruses can infect their hosts. Mammalian orthoreovirus, a human enteric virus that infects most humans during childhood, is negatively affected by antibiotic treatment prior to infection. However, it is not known how components of the host microbiota affect reovirus infectivity. In this study, we show that reovirus virions directly interact with Gram positive and Gram negative bacteria. Reovirus interaction with bacterial cells conveys enhanced virion thermostability that translates into enhanced attachment and infection of cells following an environmental insult. Enhanced virion thermostability was also conveyed by bacterial envelope components lipopolysaccharide (LPS) and peptidoglycan (PG). Lipoteichoic acid and N-acetylglucosamine-containing polysaccharides enhanced virion stability in a serotype-dependent manner. LPS and PG also enhanced the thermostability of an intermediate reovirus particle (ISVP) that is associated with primary infection in the gut. Although LPS and PG alter reovirus thermostability, these bacterial envelope components did not affect reovirus utilization of its proteinaceous cellular receptor junctional adhesion molecule-A or cell entry kinetics. LPS and PG also did not affect the overall number of reovirus capsid proteins σ1 and σ3, suggesting their effect on virion thermostability is not mediated through altering the overall number of major capsid proteins on the virus. Incubation of reovirus with LPS and PG did not significantly affect the neutralizing efficiency of reovirus-specific antibodies. These data suggest that bacteria enhance reovirus infection of the intestinal tract by enhancing the thermal stability of the reovirus particle at a variety of temperatures through interactions between the viral particle and bacterial envelope components.
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spelling pubmed-57347932017-12-22 Bacteria and bacterial envelope components enhance mammalian reovirus thermostability Berger, Angela K. Yi, Hong Kearns, Daniel B. Mainou, Bernardo A. PLoS Pathog Research Article Enteric viruses encounter diverse environments as they migrate through the gastrointestinal tract to infect their hosts. The interaction of eukaryotic viruses with members of the host microbiota can greatly impact various aspects of virus biology, including the efficiency with which viruses can infect their hosts. Mammalian orthoreovirus, a human enteric virus that infects most humans during childhood, is negatively affected by antibiotic treatment prior to infection. However, it is not known how components of the host microbiota affect reovirus infectivity. In this study, we show that reovirus virions directly interact with Gram positive and Gram negative bacteria. Reovirus interaction with bacterial cells conveys enhanced virion thermostability that translates into enhanced attachment and infection of cells following an environmental insult. Enhanced virion thermostability was also conveyed by bacterial envelope components lipopolysaccharide (LPS) and peptidoglycan (PG). Lipoteichoic acid and N-acetylglucosamine-containing polysaccharides enhanced virion stability in a serotype-dependent manner. LPS and PG also enhanced the thermostability of an intermediate reovirus particle (ISVP) that is associated with primary infection in the gut. Although LPS and PG alter reovirus thermostability, these bacterial envelope components did not affect reovirus utilization of its proteinaceous cellular receptor junctional adhesion molecule-A or cell entry kinetics. LPS and PG also did not affect the overall number of reovirus capsid proteins σ1 and σ3, suggesting their effect on virion thermostability is not mediated through altering the overall number of major capsid proteins on the virus. Incubation of reovirus with LPS and PG did not significantly affect the neutralizing efficiency of reovirus-specific antibodies. These data suggest that bacteria enhance reovirus infection of the intestinal tract by enhancing the thermal stability of the reovirus particle at a variety of temperatures through interactions between the viral particle and bacterial envelope components. Public Library of Science 2017-12-06 /pmc/articles/PMC5734793/ /pubmed/29211815 http://dx.doi.org/10.1371/journal.ppat.1006768 Text en © 2017 Berger et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Berger, Angela K.
Yi, Hong
Kearns, Daniel B.
Mainou, Bernardo A.
Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title_full Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title_fullStr Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title_full_unstemmed Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title_short Bacteria and bacterial envelope components enhance mammalian reovirus thermostability
title_sort bacteria and bacterial envelope components enhance mammalian reovirus thermostability
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5734793/
https://www.ncbi.nlm.nih.gov/pubmed/29211815
http://dx.doi.org/10.1371/journal.ppat.1006768
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