The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures

Understanding Influenza B virus infections is of critical importance in our efforts to control severe influenza and influenza-related diseases. Until 2020, two genetic lineages of influenza B virus—Yamagata and Victoria—circulated in the population. These lineages are antigenically distinct, but the...

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Main Authors: Jo L. Wilson, Elgin Akin, Ruifeng Zhou, Anne Jedlicka, Amanda Dziedzic, Hsuan Liu, Katherine Z. J. Fenstermacher, Richard E. Rothman, Andrew Pekosz
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/15/9/1956
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author Jo L. Wilson
Elgin Akin
Ruifeng Zhou
Anne Jedlicka
Amanda Dziedzic
Hsuan Liu
Katherine Z. J. Fenstermacher
Richard E. Rothman
Andrew Pekosz
author_facet Jo L. Wilson
Elgin Akin
Ruifeng Zhou
Anne Jedlicka
Amanda Dziedzic
Hsuan Liu
Katherine Z. J. Fenstermacher
Richard E. Rothman
Andrew Pekosz
author_sort Jo L. Wilson
collection DOAJ
description Understanding Influenza B virus infections is of critical importance in our efforts to control severe influenza and influenza-related diseases. Until 2020, two genetic lineages of influenza B virus—Yamagata and Victoria—circulated in the population. These lineages are antigenically distinct, but the differences in virus replication or the induction of host cell responses after infection have not been carefully studied. Recent IBV clinical isolates of both lineages were obtained from influenza surveillance efforts of the Johns Hopkins Center of Excellence in Influenza Research and Response and characterized in vitro. B/Victoria and B/Yamagata clinical isolates were recognized less efficiently by serum from influenza-vaccinated individuals in comparison to the vaccine strains. B/Victoria lineages formed smaller plaques on MDCK cells compared to B/Yamagata, but infectious virus production in primary human nasal epithelial cell (hNEC) cultures showed no differences. While ciliated epithelial cells were the dominant cell type infected by both lineages, B/Victoria lineages had a slight preference for MUC5AC-positive cells, and B/Yamagata lineages infected more basal cells. Finally, while both lineages induced a strong interferon response 48 h after infection of hNEC cultures, the B/Victoria lineages showed a much stronger induction of interferon-related signaling pathways compared to B/Yamagata. This demonstrates that the two influenza B virus lineages differ not only in their antigenic structure but also in their ability to induce host innate immune responses.
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spelling doaj.art-0c91ffc9976e4c498bd018f6a90139332023-11-19T13:24:06ZengMDPI AGViruses1999-49152023-09-01159195610.3390/v15091956The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell CulturesJo L. Wilson0Elgin Akin1Ruifeng Zhou2Anne Jedlicka3Amanda Dziedzic4Hsuan Liu5Katherine Z. J. Fenstermacher6Richard E. Rothman7Andrew Pekosz8W. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USADepartment of Emergency Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USADepartment of Emergency Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USAW. Harry Feinstone, Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USAUnderstanding Influenza B virus infections is of critical importance in our efforts to control severe influenza and influenza-related diseases. Until 2020, two genetic lineages of influenza B virus—Yamagata and Victoria—circulated in the population. These lineages are antigenically distinct, but the differences in virus replication or the induction of host cell responses after infection have not been carefully studied. Recent IBV clinical isolates of both lineages were obtained from influenza surveillance efforts of the Johns Hopkins Center of Excellence in Influenza Research and Response and characterized in vitro. B/Victoria and B/Yamagata clinical isolates were recognized less efficiently by serum from influenza-vaccinated individuals in comparison to the vaccine strains. B/Victoria lineages formed smaller plaques on MDCK cells compared to B/Yamagata, but infectious virus production in primary human nasal epithelial cell (hNEC) cultures showed no differences. While ciliated epithelial cells were the dominant cell type infected by both lineages, B/Victoria lineages had a slight preference for MUC5AC-positive cells, and B/Yamagata lineages infected more basal cells. Finally, while both lineages induced a strong interferon response 48 h after infection of hNEC cultures, the B/Victoria lineages showed a much stronger induction of interferon-related signaling pathways compared to B/Yamagata. This demonstrates that the two influenza B virus lineages differ not only in their antigenic structure but also in their ability to induce host innate immune responses.https://www.mdpi.com/1999-4915/15/9/1956influenza B virushuman nasal epithelial cellscell tropismviral transcriptomicsprotein immunoassay
spellingShingle Jo L. Wilson
Elgin Akin
Ruifeng Zhou
Anne Jedlicka
Amanda Dziedzic
Hsuan Liu
Katherine Z. J. Fenstermacher
Richard E. Rothman
Andrew Pekosz
The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
Viruses
influenza B virus
human nasal epithelial cells
cell tropism
viral transcriptomics
protein immunoassay
title The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
title_full The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
title_fullStr The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
title_full_unstemmed The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
title_short The Influenza B Virus Victoria and Yamagata Lineages Display Distinct Cell Tropism and Infection-Induced Host Gene Expression in Human Nasal Epithelial Cell Cultures
title_sort influenza b virus victoria and yamagata lineages display distinct cell tropism and infection induced host gene expression in human nasal epithelial cell cultures
topic influenza B virus
human nasal epithelial cells
cell tropism
viral transcriptomics
protein immunoassay
url https://www.mdpi.com/1999-4915/15/9/1956
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