Cargando…

Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators

The cell intrinsic antiviral response of multicellular organisms developed over millions of years and critically relies on the ability to sense and eliminate viral nucleic acids. Here we use an affinity proteomics approach in evolutionary distant species (human, mouse and fly) to identify proteins t...

Descripción completa

Detalles Bibliográficos
Autores principales: Pennemann, Friederike L., Mussabekova, Assel, Urban, Christian, Stukalov, Alexey, Andersen, Line Lykke, Grass, Vincent, Lavacca, Teresa Maria, Holze, Cathleen, Oubraham, Lila, Benamrouche, Yasmine, Girardi, Enrico, Boulos, Rasha E., Hartmann, Rune, Superti-Furga, Giulio, Habjan, Matthias, Imler, Jean-Luc, Meignin, Carine, Pichlmair, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636641/
https://www.ncbi.nlm.nih.gov/pubmed/34853303
http://dx.doi.org/10.1038/s41467-021-27192-w
_version_ 1784608568169725952
author Pennemann, Friederike L.
Mussabekova, Assel
Urban, Christian
Stukalov, Alexey
Andersen, Line Lykke
Grass, Vincent
Lavacca, Teresa Maria
Holze, Cathleen
Oubraham, Lila
Benamrouche, Yasmine
Girardi, Enrico
Boulos, Rasha E.
Hartmann, Rune
Superti-Furga, Giulio
Habjan, Matthias
Imler, Jean-Luc
Meignin, Carine
Pichlmair, Andreas
author_facet Pennemann, Friederike L.
Mussabekova, Assel
Urban, Christian
Stukalov, Alexey
Andersen, Line Lykke
Grass, Vincent
Lavacca, Teresa Maria
Holze, Cathleen
Oubraham, Lila
Benamrouche, Yasmine
Girardi, Enrico
Boulos, Rasha E.
Hartmann, Rune
Superti-Furga, Giulio
Habjan, Matthias
Imler, Jean-Luc
Meignin, Carine
Pichlmair, Andreas
author_sort Pennemann, Friederike L.
collection PubMed
description The cell intrinsic antiviral response of multicellular organisms developed over millions of years and critically relies on the ability to sense and eliminate viral nucleic acids. Here we use an affinity proteomics approach in evolutionary distant species (human, mouse and fly) to identify proteins that are conserved in their ability to associate with diverse viral nucleic acids. This approach shows a core of orthologous proteins targeting viral genetic material and species-specific interactions. Functional characterization of the influence of 181 candidates on replication of 6 distinct viruses in human cells and flies identifies 128 nucleic acid binding proteins with an impact on virus growth. We identify the family of TAO kinases (TAOK1, −2 and −3) as dsRNA-interacting antiviral proteins and show their requirement for type-I interferon induction. Depletion of TAO kinases in mammals or flies leads to an impaired response to virus infection characterized by a reduced induction of interferon stimulated genes in mammals and impaired expression of srg1 and diedel in flies. Overall, our study shows a larger set of proteins able to mediate the interaction between viral genetic material and host factors than anticipated so far, attesting to the ancestral roots of innate immunity and to the lineage-specific pressures exerted by viruses.
format Online
Article
Text
id pubmed-8636641
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-86366412021-12-15 Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators Pennemann, Friederike L. Mussabekova, Assel Urban, Christian Stukalov, Alexey Andersen, Line Lykke Grass, Vincent Lavacca, Teresa Maria Holze, Cathleen Oubraham, Lila Benamrouche, Yasmine Girardi, Enrico Boulos, Rasha E. Hartmann, Rune Superti-Furga, Giulio Habjan, Matthias Imler, Jean-Luc Meignin, Carine Pichlmair, Andreas Nat Commun Article The cell intrinsic antiviral response of multicellular organisms developed over millions of years and critically relies on the ability to sense and eliminate viral nucleic acids. Here we use an affinity proteomics approach in evolutionary distant species (human, mouse and fly) to identify proteins that are conserved in their ability to associate with diverse viral nucleic acids. This approach shows a core of orthologous proteins targeting viral genetic material and species-specific interactions. Functional characterization of the influence of 181 candidates on replication of 6 distinct viruses in human cells and flies identifies 128 nucleic acid binding proteins with an impact on virus growth. We identify the family of TAO kinases (TAOK1, −2 and −3) as dsRNA-interacting antiviral proteins and show their requirement for type-I interferon induction. Depletion of TAO kinases in mammals or flies leads to an impaired response to virus infection characterized by a reduced induction of interferon stimulated genes in mammals and impaired expression of srg1 and diedel in flies. Overall, our study shows a larger set of proteins able to mediate the interaction between viral genetic material and host factors than anticipated so far, attesting to the ancestral roots of innate immunity and to the lineage-specific pressures exerted by viruses. Nature Publishing Group UK 2021-12-01 /pmc/articles/PMC8636641/ /pubmed/34853303 http://dx.doi.org/10.1038/s41467-021-27192-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Pennemann, Friederike L.
Mussabekova, Assel
Urban, Christian
Stukalov, Alexey
Andersen, Line Lykke
Grass, Vincent
Lavacca, Teresa Maria
Holze, Cathleen
Oubraham, Lila
Benamrouche, Yasmine
Girardi, Enrico
Boulos, Rasha E.
Hartmann, Rune
Superti-Furga, Giulio
Habjan, Matthias
Imler, Jean-Luc
Meignin, Carine
Pichlmair, Andreas
Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title_full Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title_fullStr Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title_full_unstemmed Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title_short Cross-species analysis of viral nucleic acid interacting proteins identifies TAOKs as innate immune regulators
title_sort cross-species analysis of viral nucleic acid interacting proteins identifies taoks as innate immune regulators
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636641/
https://www.ncbi.nlm.nih.gov/pubmed/34853303
http://dx.doi.org/10.1038/s41467-021-27192-w
work_keys_str_mv AT pennemannfriederikel crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT mussabekovaassel crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT urbanchristian crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT stukalovalexey crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT andersenlinelykke crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT grassvincent crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT lavaccateresamaria crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT holzecathleen crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT oubrahamlila crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT benamroucheyasmine crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT girardienrico crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT boulosrashae crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT hartmannrune crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT supertifurgagiulio crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT habjanmatthias crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT imlerjeanluc crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT meignincarine crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators
AT pichlmairandreas crossspeciesanalysisofviralnucleicacidinteractingproteinsidentifiestaoksasinnateimmuneregulators