Master mitotic kinases regulate viral genome delivery during papillomavirus cell entry

Matteo Rizzato, Fuxiang Mao, Florian Chardon, Kun-Yi Lai, Ruth Villalonga-Planells, Hannes C. A. Drexler, Marion E. Pesenti, Mert Fiskin, Nora Roos, Kelly M. King, Shuaizhi Li, Eduardo R. Gamez, Lilo Greune, Petra Dersch, Claudia Simon, Murielle Masson, Koenraad Doorslaer, Samuel K. Campos and Mario Schelhaas ()
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Matteo Rizzato: Westphalian Wilhelms-University of Münster
Fuxiang Mao: Westphalian Wilhelms-University of Münster
Florian Chardon: Westphalian Wilhelms-University of Münster
Kun-Yi Lai: Westphalian Wilhelms-University of Münster
Ruth Villalonga-Planells: Westphalian Wilhelms-University of Münster
Hannes C. A. Drexler: Max Planck Institute for Molecular Biomedicine
Marion E. Pesenti: Max Planck Institute of Molecular Physiology
Mert Fiskin: UMR 7242 Biotechnologie et signalisation cellulaire, CNRS, UdS, ESBS
Nora Roos: Institute of Medical Virology and Epidemiology of Viral Diseases
Kelly M. King: University of Arizona
Shuaizhi Li: University of Arizona
Eduardo R. Gamez: University of Arizona
Lilo Greune: Westphalian Wilhelms-University of Münster
Petra Dersch: Westphalian Wilhelms-University of Münster
Claudia Simon: Institute of Medical Virology and Epidemiology of Viral Diseases
Murielle Masson: UMR 7242 Biotechnologie et signalisation cellulaire, CNRS, UdS, ESBS
Koenraad Doorslaer: University of Arizona
Samuel K. Campos: University of Arizona
Mario Schelhaas: Westphalian Wilhelms-University of Münster

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract Mitosis induces cellular rearrangements like spindle formation, Golgi fragmentation, and nuclear envelope breakdown. Similar to certain retroviruses, nuclear delivery during entry of human papillomavirus (HPV) genomes is facilitated by mitosis, during which minor capsid protein L2 tethers viral DNA to mitotic chromosomes. However, the mechanism of viral genome delivery and tethering to condensed chromosomes is barely understood. It is unclear, which cellular proteins facilitate this process or how this process is regulated. This work identifies crucial phosphorylations on HPV minor capsid protein L2 occurring at mitosis onset. L2’s chromosome binding region (CBR) is sequentially phosphorylated by the master mitotic kinases CDK1 and PLK1. L2 phosphorylation, thus, regulates timely delivery of HPV vDNA to mitotic chromatin during mitosis. In summary, our work demonstrates a crucial role of mitotic kinases for nuclear delivery of viral DNA and provides important insights into the molecular mechanism of pathogen import into the nucleus during mitosis.

Date: 2023
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DOI: 10.1038/s41467-023-35874-w

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