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Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination

Ebola virus (EBOV) disease is marked by rapid virus replication and spread. EBOV enters the cell by macropinocytosis and replicates in the cytoplasm, and nascent virions egress from the cell surface to infect neighboring cells. Here, we show that EBOV uses an alternate route to disseminate: tunnelin...

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Autores principales: Djurkovic, Marija A, Leavitt, Carson G, Arnett, Eusondia, Kriachun, Valeriia, Martínez-Sobrido, Luis, Titone, Rossella, Sherwood, Laura J, Hayhurst, Andrew, Schlesinger, Larry S, Shtanko, Olena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651192/
https://www.ncbi.nlm.nih.gov/pubmed/37723997
http://dx.doi.org/10.1093/infdis/jiad400
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author Djurkovic, Marija A
Leavitt, Carson G
Arnett, Eusondia
Kriachun, Valeriia
Martínez-Sobrido, Luis
Titone, Rossella
Sherwood, Laura J
Hayhurst, Andrew
Schlesinger, Larry S
Shtanko, Olena
author_facet Djurkovic, Marija A
Leavitt, Carson G
Arnett, Eusondia
Kriachun, Valeriia
Martínez-Sobrido, Luis
Titone, Rossella
Sherwood, Laura J
Hayhurst, Andrew
Schlesinger, Larry S
Shtanko, Olena
author_sort Djurkovic, Marija A
collection PubMed
description Ebola virus (EBOV) disease is marked by rapid virus replication and spread. EBOV enters the cell by macropinocytosis and replicates in the cytoplasm, and nascent virions egress from the cell surface to infect neighboring cells. Here, we show that EBOV uses an alternate route to disseminate: tunneling nanotubes (TNTs). TNTs, an actin-based long-range intercellular communication system, allows for direct exchange of cytosolic constituents between cells. Using live, scanning electron, and high-resolution quantitative 3-dimensional microscopy, we show that EBOV infection of primary human cells results in the enhanced formation of TNTs containing viral nucleocapsids. TNTs promote the intercellular transfer of nucleocapsids in the absence of live virus, and virus could replicate in cells devoid of entry factors after initial stall. Our studies suggest an alternate model of EBOV dissemination within the host, laying the groundwork for further investigations into the pathogenesis of filoviruses and, importantly, stimulating new areas of antiviral design.
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spelling pubmed-106511922023-09-19 Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination Djurkovic, Marija A Leavitt, Carson G Arnett, Eusondia Kriachun, Valeriia Martínez-Sobrido, Luis Titone, Rossella Sherwood, Laura J Hayhurst, Andrew Schlesinger, Larry S Shtanko, Olena J Infect Dis Supplement Article Ebola virus (EBOV) disease is marked by rapid virus replication and spread. EBOV enters the cell by macropinocytosis and replicates in the cytoplasm, and nascent virions egress from the cell surface to infect neighboring cells. Here, we show that EBOV uses an alternate route to disseminate: tunneling nanotubes (TNTs). TNTs, an actin-based long-range intercellular communication system, allows for direct exchange of cytosolic constituents between cells. Using live, scanning electron, and high-resolution quantitative 3-dimensional microscopy, we show that EBOV infection of primary human cells results in the enhanced formation of TNTs containing viral nucleocapsids. TNTs promote the intercellular transfer of nucleocapsids in the absence of live virus, and virus could replicate in cells devoid of entry factors after initial stall. Our studies suggest an alternate model of EBOV dissemination within the host, laying the groundwork for further investigations into the pathogenesis of filoviruses and, importantly, stimulating new areas of antiviral design. Oxford University Press 2023-09-19 /pmc/articles/PMC10651192/ /pubmed/37723997 http://dx.doi.org/10.1093/infdis/jiad400 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Infectious Diseases Society of America. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Supplement Article
Djurkovic, Marija A
Leavitt, Carson G
Arnett, Eusondia
Kriachun, Valeriia
Martínez-Sobrido, Luis
Titone, Rossella
Sherwood, Laura J
Hayhurst, Andrew
Schlesinger, Larry S
Shtanko, Olena
Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title_full Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title_fullStr Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title_full_unstemmed Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title_short Ebola Virus Uses Tunneling Nanotubes as an Alternate Route of Dissemination
title_sort ebola virus uses tunneling nanotubes as an alternate route of dissemination
topic Supplement Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651192/
https://www.ncbi.nlm.nih.gov/pubmed/37723997
http://dx.doi.org/10.1093/infdis/jiad400
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