The host RNA polymerase II C-terminal domain is the anchor for replication of the influenza virus genome

Tim Krischuns (), Benoît Arragain, Catherine Isel, Sylvain Paisant, Matthias Budt, Thorsten Wolff, Stephen Cusack () and Nadia Naffakh ()
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Tim Krischuns: Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus
Benoît Arragain: European Molecular Biology Laboratory
Catherine Isel: Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus
Sylvain Paisant: Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus
Matthias Budt: Robert Koch Institut
Thorsten Wolff: Robert Koch Institut
Stephen Cusack: European Molecular Biology Laboratory
Nadia Naffakh: Université Paris Cité, CNRS UMR 3569, RNA Biology of Influenza Virus

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract The current model is that the influenza virus polymerase (FluPol) binds either to host RNA polymerase II (RNAP II) or to the acidic nuclear phosphoprotein 32 (ANP32), which drives its conformation and activity towards transcription or replication of the viral genome, respectively. Here, we provide evidence that the FluPol-RNAP II binding interface, beyond its well-acknowledged function in cap-snatching during transcription initiation, has also a pivotal role in replication of the viral genome. Using a combination of cell-based and in vitro approaches, we show that the RNAP II C-terminal-domain, jointly with ANP32, enhances FluPol replication activity. We observe successive conformational changes to switch from a transcriptase to a replicase conformation in the presence of the bound RNPAII C-terminal domain and propose a model in which the host RNAP II is the anchor for transcription and replication of the viral genome. Our data open new perspectives on the spatial coupling of viral transcription and replication and the coordinated balance between these two activities.

Date: 2024
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DOI: 10.1038/s41467-024-45205-2

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