Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection

Skeletal muscle, at 30 to 40% of body mass, is the most abundant soft tissue in the body. Besides its primary function in movement and posture, skeletal muscle is a significant innate immune organ with the capacity to produce cytokines and chemokines and respond to proinflammatory cytokines. Little...

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Main Authors: Baquero-Perez, Belinda, Kuchipudi, Suresh V., Ho, Jemima, Sebastian, Sujith, Puranik, Anita, Howard, Wendy, Brookes, Sharon M., Brown, Ian H., Chang, Kin-Chow
Format: Article
Published: American Society for Microbiology 2015
Online Access:https://eprints.nottingham.ac.uk/43918/
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author Baquero-Perez, Belinda
Kuchipudi, Suresh V.
Ho, Jemima
Sebastian, Sujith
Puranik, Anita
Howard, Wendy
Brookes, Sharon M.
Brown, Ian H.
Chang, Kin-Chow
author_facet Baquero-Perez, Belinda
Kuchipudi, Suresh V.
Ho, Jemima
Sebastian, Sujith
Puranik, Anita
Howard, Wendy
Brookes, Sharon M.
Brown, Ian H.
Chang, Kin-Chow
author_sort Baquero-Perez, Belinda
building Nottingham Research Data Repository
collection Online Access
description Skeletal muscle, at 30 to 40% of body mass, is the most abundant soft tissue in the body. Besides its primary function in movement and posture, skeletal muscle is a significant innate immune organ with the capacity to produce cytokines and chemokines and respond to proinflammatory cytokines. Little is known about the role of skeletal muscle during systemic influenza A virus infection in any host and particularly avian species. Here we used primary chicken and duck multinucleated myotubes to examine their susceptibility and innate immune response to influenza virus infections. Both chicken and duck myotubes expressed avian and human sialic acid receptors and were readily susceptible to low-pathogenicity (H2N3 A/mallard duck/England/7277/06) and high-pathogenicity (H5N1 A/turkey/England/50-92/91 and H5N1 A/turkey/Turkey/1/05) avian and human H1N1 (A/USSR/77) influenza viruses. Both avian host species produced comparable levels of progeny H5N1 A/turkey/Turkey/1/05 virus.Notably, the rapid accumulation of viral nucleoprotein and matrix (M) gene RNA in chicken and duck myotubes was accompanied by extensive cytopathic damage with marked myotube apoptosis (widespread microscopic blebs, caspase 3/7 activation, and annexin V binding at the plasma membrane). Infected chicken myotubes produced significantly higher levels of proinflammatory cytokines than did the corresponding duck cells. Additionally, in chicken myotubes infected with H5N1 viruses, the induction of interferon beta (IFN-beta) and IFN-inducible genes, including the melanoma differentiation-associated protein 5 (MDA-5) gene, was relatively weak compared to infection with the corresponding H2N3 virus. Our findings highlight that avian skeletal muscle fibers are capable of productive influenza virus replication and are a potential tissue source of infection.
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spelling nottingham-439182020-05-04T17:01:35Z https://eprints.nottingham.ac.uk/43918/ Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection Baquero-Perez, Belinda Kuchipudi, Suresh V. Ho, Jemima Sebastian, Sujith Puranik, Anita Howard, Wendy Brookes, Sharon M. Brown, Ian H. Chang, Kin-Chow Skeletal muscle, at 30 to 40% of body mass, is the most abundant soft tissue in the body. Besides its primary function in movement and posture, skeletal muscle is a significant innate immune organ with the capacity to produce cytokines and chemokines and respond to proinflammatory cytokines. Little is known about the role of skeletal muscle during systemic influenza A virus infection in any host and particularly avian species. Here we used primary chicken and duck multinucleated myotubes to examine their susceptibility and innate immune response to influenza virus infections. Both chicken and duck myotubes expressed avian and human sialic acid receptors and were readily susceptible to low-pathogenicity (H2N3 A/mallard duck/England/7277/06) and high-pathogenicity (H5N1 A/turkey/England/50-92/91 and H5N1 A/turkey/Turkey/1/05) avian and human H1N1 (A/USSR/77) influenza viruses. Both avian host species produced comparable levels of progeny H5N1 A/turkey/Turkey/1/05 virus.Notably, the rapid accumulation of viral nucleoprotein and matrix (M) gene RNA in chicken and duck myotubes was accompanied by extensive cytopathic damage with marked myotube apoptosis (widespread microscopic blebs, caspase 3/7 activation, and annexin V binding at the plasma membrane). Infected chicken myotubes produced significantly higher levels of proinflammatory cytokines than did the corresponding duck cells. Additionally, in chicken myotubes infected with H5N1 viruses, the induction of interferon beta (IFN-beta) and IFN-inducible genes, including the melanoma differentiation-associated protein 5 (MDA-5) gene, was relatively weak compared to infection with the corresponding H2N3 virus. Our findings highlight that avian skeletal muscle fibers are capable of productive influenza virus replication and are a potential tissue source of infection. American Society for Microbiology 2015-03-01 Article PeerReviewed Baquero-Perez, Belinda, Kuchipudi, Suresh V., Ho, Jemima, Sebastian, Sujith, Puranik, Anita, Howard, Wendy, Brookes, Sharon M., Brown, Ian H. and Chang, Kin-Chow (2015) Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection. Journal of Virology, 89 (5). pp. 2494-2506. ISSN 0022-538X http://jvi.asm.org/content/89/5/2494 doi:10.1128/JVI.03421-14 doi:10.1128/JVI.03421-14
spellingShingle Baquero-Perez, Belinda
Kuchipudi, Suresh V.
Ho, Jemima
Sebastian, Sujith
Puranik, Anita
Howard, Wendy
Brookes, Sharon M.
Brown, Ian H.
Chang, Kin-Chow
Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title_full Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title_fullStr Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title_full_unstemmed Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title_short Chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
title_sort chicken and duck myotubes are highly susceptible and permissive to influenza virus infection
url https://eprints.nottingham.ac.uk/43918/
https://eprints.nottingham.ac.uk/43918/
https://eprints.nottingham.ac.uk/43918/