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

Friederike L. Pennemann, Assel Mussabekova, Christian Urban, Alexey Stukalov, Line Lykke Andersen, Vincent Grass, Teresa Maria Lavacca, Cathleen Holze, Lila Oubraham, Yasmine Benamrouche, Enrico Girardi, Rasha E. Boulos, Rune Hartmann, Giulio Superti-Furga, Matthias Habjan, Jean-Luc Imler, Carine Meignin and Andreas Pichlmair ()
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Friederike L. Pennemann: Technical University of Munich, School of Medicine, Institute of Virology
Assel Mussabekova: Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire
Christian Urban: Technical University of Munich, School of Medicine, Institute of Virology
Alexey Stukalov: Technical University of Munich, School of Medicine, Institute of Virology
Line Lykke Andersen: Technical University of Munich, School of Medicine, Institute of Virology
Vincent Grass: Technical University of Munich, School of Medicine, Institute of Virology
Teresa Maria Lavacca: Technical University of Munich, School of Medicine, Institute of Virology
Cathleen Holze: Innate Immunity Laboratory, Max-Planck Institute of Biochemistry
Lila Oubraham: Technical University of Munich, School of Medicine, Institute of Virology
Yasmine Benamrouche: Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire
Enrico Girardi: CeMM - Center for Molecular Medicine of the Austrian Academy of Sciences
Rasha E. Boulos: Lebanese American University
Rune Hartmann: Aarhus University, Department of Molecular Biology and Genetics - Structural Biology
Giulio Superti-Furga: CeMM - Center for Molecular Medicine of the Austrian Academy of Sciences
Matthias Habjan: Innate Immunity Laboratory, Max-Planck Institute of Biochemistry
Jean-Luc Imler: Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire
Carine Meignin: Université de Strasbourg, CNRS UPR9022, Institut de Biologie Moléculaire et Cellulaire
Andreas Pichlmair: Technical University of Munich, School of Medicine, Institute of Virology

Nature Communications, 2021, vol. 12, issue 1, 1-22

Abstract: Abstract 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.

Date: 2021
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DOI: 10.1038/s41467-021-27192-w

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