Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants

Influenza A viruses (IAV) cause annual epidemics and occasional pandemics in humans. The most recent pandemic outbreak occurred in 2009 with H1N1pdm09. This virus, which most likely reassorted in swine before its transmission to humans, was reintroduced into the swine population and continues circul...

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Main Authors: Verónica A. Ferrando, Marcel E. Friedrich, Shrey Gandhi, Alexander Mellmann, Dörthe Masemann, Anmari Christersson, Darisuren Anhlan, Linda Brunotte, Monika Stoll, Timm Harder, Martin Beer, Yvonne Boergeling, Stephan Ludwig
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2023.2212809
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author Verónica A. Ferrando
Marcel E. Friedrich
Shrey Gandhi
Alexander Mellmann
Dörthe Masemann
Anmari Christersson
Darisuren Anhlan
Linda Brunotte
Monika Stoll
Timm Harder
Martin Beer
Yvonne Boergeling
Stephan Ludwig
author_facet Verónica A. Ferrando
Marcel E. Friedrich
Shrey Gandhi
Alexander Mellmann
Dörthe Masemann
Anmari Christersson
Darisuren Anhlan
Linda Brunotte
Monika Stoll
Timm Harder
Martin Beer
Yvonne Boergeling
Stephan Ludwig
author_sort Verónica A. Ferrando
collection DOAJ
description Influenza A viruses (IAV) cause annual epidemics and occasional pandemics in humans. The most recent pandemic outbreak occurred in 2009 with H1N1pdm09. This virus, which most likely reassorted in swine before its transmission to humans, was reintroduced into the swine population and continues circulating ever since. In order to assess its potential to cause reassortants on a cellular level, human origin H1N1pdm09 and a recent Eurasian avian-like H1N1 swine IAV were (co-)passaged in the newly generated swine lung cell line C22. Co-infection with both viruses gave rise to numerous reassortants that additionally carry different mutations which can partially be found in nature as well. Reassortment most frequently affected the PB1, PA and NA segments with the swine IAV as recipient. These reassortants reached higher titers in swine lung cells and were able to replicate in genuine human lung tissue explants ex vivo, suggesting a possible zoonotic potential. Interestingly, reassortment and mutations in the viral ribonucleoprotein complex influence the viral polymerase activity in a cell type and species-specific manner. In summary, we demonstrate reassortment promiscuity of these viruses in a novel swine lung cell model and indicate a possible zoonotic potential of the reassortants.
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spelling doaj-art-4a0d20eb3cce4efea4caca01d4f9af782025-08-20T01:49:16ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112110.1080/22221751.2023.2212809Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variantsVerónica A. Ferrando0Marcel E. Friedrich1Shrey Gandhi2Alexander Mellmann3Dörthe Masemann4Anmari Christersson5Darisuren Anhlan6Linda Brunotte7Monika Stoll8Timm Harder9Martin Beer10Yvonne Boergeling11Stephan Ludwig12Institute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyDepartment of Genetic Epidemiology, Institute of Human Genetics, Westfälische Wilhelms-University, Münster, GermanyInstitute of Hygiene Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyDepartment of Genetic Epidemiology, Institute of Human Genetics, Westfälische Wilhelms-University, Münster, GermanyInstitute of Diagnostic Virology, Friedrich-Loeffler-Institute, Greifswald, GermanyInstitute of Diagnostic Virology, Friedrich-Loeffler-Institute, Greifswald, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInstitute of Virology Münster, Westfälische Wilhelms-University, Münster, GermanyInfluenza A viruses (IAV) cause annual epidemics and occasional pandemics in humans. The most recent pandemic outbreak occurred in 2009 with H1N1pdm09. This virus, which most likely reassorted in swine before its transmission to humans, was reintroduced into the swine population and continues circulating ever since. In order to assess its potential to cause reassortants on a cellular level, human origin H1N1pdm09 and a recent Eurasian avian-like H1N1 swine IAV were (co-)passaged in the newly generated swine lung cell line C22. Co-infection with both viruses gave rise to numerous reassortants that additionally carry different mutations which can partially be found in nature as well. Reassortment most frequently affected the PB1, PA and NA segments with the swine IAV as recipient. These reassortants reached higher titers in swine lung cells and were able to replicate in genuine human lung tissue explants ex vivo, suggesting a possible zoonotic potential. Interestingly, reassortment and mutations in the viral ribonucleoprotein complex influence the viral polymerase activity in a cell type and species-specific manner. In summary, we demonstrate reassortment promiscuity of these viruses in a novel swine lung cell model and indicate a possible zoonotic potential of the reassortants.https://www.tandfonline.com/doi/10.1080/22221751.2023.2212809Zoonosisswineinfluenza virusreassortmentevolution
spellingShingle Verónica A. Ferrando
Marcel E. Friedrich
Shrey Gandhi
Alexander Mellmann
Dörthe Masemann
Anmari Christersson
Darisuren Anhlan
Linda Brunotte
Monika Stoll
Timm Harder
Martin Beer
Yvonne Boergeling
Stephan Ludwig
Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
Emerging Microbes and Infections
Zoonosis
swine
influenza virus
reassortment
evolution
title Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
title_full Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
title_fullStr Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
title_full_unstemmed Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
title_short Cell-intrinsic genomic reassortment of pandemic H1N1 2009 and Eurasian avian-like swine influenza viruses results in potentially zoonotic variants
title_sort cell intrinsic genomic reassortment of pandemic h1n1 2009 and eurasian avian like swine influenza viruses results in potentially zoonotic variants
topic Zoonosis
swine
influenza virus
reassortment
evolution
url https://www.tandfonline.com/doi/10.1080/22221751.2023.2212809
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