Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo

In order to better understand differences in the outcome of infectious bursal disease virus (IBDV) infection, we inoculated a very virulent (vv) strain into White Leghorn chickens of inbred line W that was previously reported to experience over 24% flock mortality, and three inbred lines (15I, C.B4...

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Main Authors: Amin S. Asfor, Salik Nazki, Vishwanatha R.A.P. Reddy, Elle Campbell, Katherine L. Dulwich, Efstathios S. Giotis, Michael A. Skinner, Andrew J. Broadbent
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/13/5/933
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author Amin S. Asfor
Salik Nazki
Vishwanatha R.A.P. Reddy
Elle Campbell
Katherine L. Dulwich
Efstathios S. Giotis
Michael A. Skinner
Andrew J. Broadbent
author_facet Amin S. Asfor
Salik Nazki
Vishwanatha R.A.P. Reddy
Elle Campbell
Katherine L. Dulwich
Efstathios S. Giotis
Michael A. Skinner
Andrew J. Broadbent
author_sort Amin S. Asfor
collection DOAJ
description In order to better understand differences in the outcome of infectious bursal disease virus (IBDV) infection, we inoculated a very virulent (vv) strain into White Leghorn chickens of inbred line W that was previously reported to experience over 24% flock mortality, and three inbred lines (15I, C.B4 and 0) that were previously reported to display no mortality. Within each experimental group, some individuals experienced more severe disease than others but line 15I birds experienced milder disease based on average clinical scores, percentage of birds with gross pathology, average bursal lesion scores and average peak bursal virus titre. RNA-Seq analysis revealed that more severe disease in line W was associated with significant up-regulation of pathways involved in inflammation, cytoskeletal regulation by Rho GTPases, nicotinic acetylcholine receptor signaling, and Wnt signaling in the bursa compared to line 15I. Primary bursal cell populations isolated from uninfected line W birds contained a significantly greater percentage of KUL01+ macrophages than cells isolated from line 15I birds (<i>p</i> < 0.01) and, when stimulated ex vivo with LPS, showed more rapid up-regulation of pro-inflammatory gene expression than those from line 15I birds. We hypothesize that a more rapid induction of pro-inflammatory cytokine responses in bursal cells following IBDV infection leads to more severe disease in line W birds than in line 15I.
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spelling doaj.art-22e5f37bcd7445498634323e93e1d0f32023-11-21T20:13:57ZengMDPI AGViruses1999-49152021-05-0113593310.3390/v13050933Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex VivoAmin S. Asfor0Salik Nazki1Vishwanatha R.A.P. Reddy2Elle Campbell3Katherine L. Dulwich4Efstathios S. Giotis5Michael A. Skinner6Andrew J. Broadbent7Birnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKBirnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKBirnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKBirnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKBirnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKSection of Virology, Faculty of Medicine, Imperial College London, St. Mary’s Campus, Norfolk Place, London W2 1PG, UKSection of Virology, Faculty of Medicine, Imperial College London, St. Mary’s Campus, Norfolk Place, London W2 1PG, UKBirnaviruses Group, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UKIn order to better understand differences in the outcome of infectious bursal disease virus (IBDV) infection, we inoculated a very virulent (vv) strain into White Leghorn chickens of inbred line W that was previously reported to experience over 24% flock mortality, and three inbred lines (15I, C.B4 and 0) that were previously reported to display no mortality. Within each experimental group, some individuals experienced more severe disease than others but line 15I birds experienced milder disease based on average clinical scores, percentage of birds with gross pathology, average bursal lesion scores and average peak bursal virus titre. RNA-Seq analysis revealed that more severe disease in line W was associated with significant up-regulation of pathways involved in inflammation, cytoskeletal regulation by Rho GTPases, nicotinic acetylcholine receptor signaling, and Wnt signaling in the bursa compared to line 15I. Primary bursal cell populations isolated from uninfected line W birds contained a significantly greater percentage of KUL01+ macrophages than cells isolated from line 15I birds (<i>p</i> < 0.01) and, when stimulated ex vivo with LPS, showed more rapid up-regulation of pro-inflammatory gene expression than those from line 15I birds. We hypothesize that a more rapid induction of pro-inflammatory cytokine responses in bursal cells following IBDV infection leads to more severe disease in line W birds than in line 15I.https://www.mdpi.com/1999-4915/13/5/933IBDVinfectious bursal diseasebursa of Fabriciusinbred lineschickens
spellingShingle Amin S. Asfor
Salik Nazki
Vishwanatha R.A.P. Reddy
Elle Campbell
Katherine L. Dulwich
Efstathios S. Giotis
Michael A. Skinner
Andrew J. Broadbent
Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
Viruses
IBDV
infectious bursal disease
bursa of Fabricius
inbred lines
chickens
title Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
title_full Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
title_fullStr Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
title_full_unstemmed Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
title_short Transcriptomic Analysis of Inbred Chicken Lines Reveals Infectious Bursal Disease Severity Is Associated with Greater Bursal Inflammation In Vivo and More Rapid Induction of Pro-Inflammatory Responses in Primary Bursal Cells Stimulated Ex Vivo
title_sort transcriptomic analysis of inbred chicken lines reveals infectious bursal disease severity is associated with greater bursal inflammation in vivo and more rapid induction of pro inflammatory responses in primary bursal cells stimulated ex vivo
topic IBDV
infectious bursal disease
bursa of Fabricius
inbred lines
chickens
url https://www.mdpi.com/1999-4915/13/5/933
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