Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.

Cellular RNA-binding proteins (RBPs) are pivotal for the viral lifecycle, mediating key host-virus interactions that promote or repress virus infection. While these interactions have been largely studied in the vertebrate host, no comprehensive analyses of protein-RNA interactions occurring in cells...

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Main Authors: Alexandra Wilson, Wael Kamel, Kelsey Davies, Zaydah R De Laurent, Rozeena Arif, Andrew T Clarke, Lesley Bell-Sakyi, Douglas Lamont, Yana Demyanenko, Marko Noerenberg, Alain Kohl, Shabaz Mohammed, Alfredo Castello, Benjamin Brennan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-08-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1013393
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author Alexandra Wilson
Wael Kamel
Kelsey Davies
Zaydah R De Laurent
Rozeena Arif
Andrew T Clarke
Lesley Bell-Sakyi
Douglas Lamont
Yana Demyanenko
Marko Noerenberg
Alain Kohl
Shabaz Mohammed
Alfredo Castello
Benjamin Brennan
author_facet Alexandra Wilson
Wael Kamel
Kelsey Davies
Zaydah R De Laurent
Rozeena Arif
Andrew T Clarke
Lesley Bell-Sakyi
Douglas Lamont
Yana Demyanenko
Marko Noerenberg
Alain Kohl
Shabaz Mohammed
Alfredo Castello
Benjamin Brennan
author_sort Alexandra Wilson
collection DOAJ
description Cellular RNA-binding proteins (RBPs) are pivotal for the viral lifecycle, mediating key host-virus interactions that promote or repress virus infection. While these interactions have been largely studied in the vertebrate host, no comprehensive analyses of protein-RNA interactions occurring in cells of arbovirus vectors, in particular ticks, have been performed to date. Here we systematically identified the responses of the RNA-binding proteome (RBPome) to infection with a prototype bunyavirus (Uukuniemi virus; UUKV) in tick cells and discovered changes in RNA-binding activity for 283 proteins. In an orthogonal approach, we analysed the composition of the viral ribonucleoprotein by immunoprecipitation of UUKV nucleocapsid protein (N) in infected cells. We found many tick RBPs that are regulated by UUKV infection and associate with viral nucleocapsid protein complexes, and we confirmed experimentally that they impact UUKV infection. This includes the tick homolog of topoisomerase 3B (TOP3B), a protein able to manipulate the topology of RNA, which particularly affected viral particle production. Our data thus reveals the first protein-RNA interaction map for infected tick cells.
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institution Kabale University
issn 1553-7366
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language English
publishDate 2025-08-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj-art-eb20d125572f48a1b9256c10491a8d7f2025-08-23T05:31:24ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-08-01218e101339310.1371/journal.ppat.1013393Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.Alexandra WilsonWael KamelKelsey DaviesZaydah R De LaurentRozeena ArifAndrew T ClarkeLesley Bell-SakyiDouglas LamontYana DemyanenkoMarko NoerenbergAlain KohlShabaz MohammedAlfredo CastelloBenjamin BrennanCellular RNA-binding proteins (RBPs) are pivotal for the viral lifecycle, mediating key host-virus interactions that promote or repress virus infection. While these interactions have been largely studied in the vertebrate host, no comprehensive analyses of protein-RNA interactions occurring in cells of arbovirus vectors, in particular ticks, have been performed to date. Here we systematically identified the responses of the RNA-binding proteome (RBPome) to infection with a prototype bunyavirus (Uukuniemi virus; UUKV) in tick cells and discovered changes in RNA-binding activity for 283 proteins. In an orthogonal approach, we analysed the composition of the viral ribonucleoprotein by immunoprecipitation of UUKV nucleocapsid protein (N) in infected cells. We found many tick RBPs that are regulated by UUKV infection and associate with viral nucleocapsid protein complexes, and we confirmed experimentally that they impact UUKV infection. This includes the tick homolog of topoisomerase 3B (TOP3B), a protein able to manipulate the topology of RNA, which particularly affected viral particle production. Our data thus reveals the first protein-RNA interaction map for infected tick cells.https://doi.org/10.1371/journal.ppat.1013393
spellingShingle Alexandra Wilson
Wael Kamel
Kelsey Davies
Zaydah R De Laurent
Rozeena Arif
Andrew T Clarke
Lesley Bell-Sakyi
Douglas Lamont
Yana Demyanenko
Marko Noerenberg
Alain Kohl
Shabaz Mohammed
Alfredo Castello
Benjamin Brennan
Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
PLoS Pathogens
title Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
title_full Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
title_fullStr Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
title_full_unstemmed Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
title_short Uukuniemi virus infection causes a pervasive remodelling of the RNA-binding proteome in tick cells.
title_sort uukuniemi virus infection causes a pervasive remodelling of the rna binding proteome in tick cells
url https://doi.org/10.1371/journal.ppat.1013393
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