Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination

ABSTRACT Immune response is a highly coordinated cascade involving all the subsets of peripheral blood mononuclear cells (PBMCs). In this study, RNA sequencing (RNA-Seq) analysis of PBMC subsets was done to delineate the systems biology behind immune protection of the vaccine in sheep and goats. The...

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Autores principales: Sajad Ahmad Wani, Manas Ranjan Praharaj, Amit R. Sahu, Raja Ishaq Nabi Khan, Shikha Saxena, Kaushal Kishor Rajak, Dhanavelu Muthuchelvan, Aditya Sahoo, Bina Mishra, Raj Kumar Singh, Bishnu Prasad Mishra, Ravi Kumar Gandham
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:39bb349a83994aa887bf309b22dbd0752021-12-02T19:36:39ZSystems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination10.1128/mSystems.00820-202379-5077https://doaj.org/article/39bb349a83994aa887bf309b22dbd0752021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00820-20https://doaj.org/toc/2379-5077ABSTRACT Immune response is a highly coordinated cascade involving all the subsets of peripheral blood mononuclear cells (PBMCs). In this study, RNA sequencing (RNA-Seq) analysis of PBMC subsets was done to delineate the systems biology behind immune protection of the vaccine in sheep and goats. The PBMC subsets studied were CD4+, CD8+, CD14+, CD21+, and CD335+ cells from day 0 and day 5 of sheep and goats vaccinated with Sungri/96 peste des petits ruminants virus. Assessment of the immune response processes enriched by the differentially expressed genes (DEGs) in all the subsets suggested a strong dysregulation toward the development of early inflammatory microenvironment, which is very much required for differentiation of monocytes to macrophages, and activation as well as the migration of dendritic cells into the draining lymph nodes. The protein-protein interaction networks among the antiviral molecules (IFIT3, ISG15, MX1, MX2, RSAD2, ISG20, IFIT5, and IFIT1) and common DEGs across PBMC subsets in both species identified ISG15 to be a ubiquitous hub that helps in orchestrating antiviral host response against peste des petits ruminants virus (PPRV). IRF7 was found to be the key master regulator activated in most of the subsets in sheep and goats. Most of the pathways were found to be inactivated in B lymphocytes of both the species, indicating that 5 days postvaccination (dpv) is too early a time point for the B lymphocytes to react. The cell-mediated immune response and humoral immune response pathways were found more enriched in goats than in sheep. Although animals from both species survived the challenge, a contrast in pathway activation was observed in CD335+ cells. IMPORTANCE Peste des petits ruminants (PPR) by PPR virus (PPRV) is an World Organisation for Animal Health (OIE)-listed acute, contagious transboundary viral disease of small ruminants. The attenuated Sungri/96 PPRV vaccine used all over India against this PPR provides long-lasting robust innate and adaptive immune response. The early antiviral response was found mediated through type I interferon-independent interferon-stimulated gene (ISG) expression. However, systems biology behind this immune response is unknown. In this study, in vivo transcriptome profiling of PBMC subsets (CD4+, CD8+, CD14+, CD21+, and CD335+) in vaccinated goats and sheep (at 5 days postvaccination) was done to understand this systems biology. Though there are a few differences in the systems biology across cells (specially the NK cells) between sheep and goats, the coordinated response that is inclusive of all the cell subsets was found to be toward the induction of a strong innate immune response, which is needed for an appropriate adaptive immune response.Sajad Ahmad WaniManas Ranjan PraharajAmit R. SahuRaja Ishaq Nabi KhanShikha SaxenaKaushal Kishor RajakDhanavelu MuthuchelvanAditya SahooBina MishraRaj Kumar SinghBishnu Prasad MishraRavi Kumar GandhamAmerican Society for MicrobiologyarticleISG15PBMCsPeste des petits ruminantsSungri/96 PPRVMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution DOAJ
collection DOAJ
language EN
topic ISG15
PBMCs
Peste des petits ruminants
Sungri/96 PPRV
Microbiology
QR1-502
spellingShingle ISG15
PBMCs
Peste des petits ruminants
Sungri/96 PPRV
Microbiology
QR1-502
Sajad Ahmad Wani
Manas Ranjan Praharaj
Amit R. Sahu
Raja Ishaq Nabi Khan
Shikha Saxena
Kaushal Kishor Rajak
Dhanavelu Muthuchelvan
Aditya Sahoo
Bina Mishra
Raj Kumar Singh
Bishnu Prasad Mishra
Ravi Kumar Gandham
Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
description ABSTRACT Immune response is a highly coordinated cascade involving all the subsets of peripheral blood mononuclear cells (PBMCs). In this study, RNA sequencing (RNA-Seq) analysis of PBMC subsets was done to delineate the systems biology behind immune protection of the vaccine in sheep and goats. The PBMC subsets studied were CD4+, CD8+, CD14+, CD21+, and CD335+ cells from day 0 and day 5 of sheep and goats vaccinated with Sungri/96 peste des petits ruminants virus. Assessment of the immune response processes enriched by the differentially expressed genes (DEGs) in all the subsets suggested a strong dysregulation toward the development of early inflammatory microenvironment, which is very much required for differentiation of monocytes to macrophages, and activation as well as the migration of dendritic cells into the draining lymph nodes. The protein-protein interaction networks among the antiviral molecules (IFIT3, ISG15, MX1, MX2, RSAD2, ISG20, IFIT5, and IFIT1) and common DEGs across PBMC subsets in both species identified ISG15 to be a ubiquitous hub that helps in orchestrating antiviral host response against peste des petits ruminants virus (PPRV). IRF7 was found to be the key master regulator activated in most of the subsets in sheep and goats. Most of the pathways were found to be inactivated in B lymphocytes of both the species, indicating that 5 days postvaccination (dpv) is too early a time point for the B lymphocytes to react. The cell-mediated immune response and humoral immune response pathways were found more enriched in goats than in sheep. Although animals from both species survived the challenge, a contrast in pathway activation was observed in CD335+ cells. IMPORTANCE Peste des petits ruminants (PPR) by PPR virus (PPRV) is an World Organisation for Animal Health (OIE)-listed acute, contagious transboundary viral disease of small ruminants. The attenuated Sungri/96 PPRV vaccine used all over India against this PPR provides long-lasting robust innate and adaptive immune response. The early antiviral response was found mediated through type I interferon-independent interferon-stimulated gene (ISG) expression. However, systems biology behind this immune response is unknown. In this study, in vivo transcriptome profiling of PBMC subsets (CD4+, CD8+, CD14+, CD21+, and CD335+) in vaccinated goats and sheep (at 5 days postvaccination) was done to understand this systems biology. Though there are a few differences in the systems biology across cells (specially the NK cells) between sheep and goats, the coordinated response that is inclusive of all the cell subsets was found to be toward the induction of a strong innate immune response, which is needed for an appropriate adaptive immune response.
format article
author Sajad Ahmad Wani
Manas Ranjan Praharaj
Amit R. Sahu
Raja Ishaq Nabi Khan
Shikha Saxena
Kaushal Kishor Rajak
Dhanavelu Muthuchelvan
Aditya Sahoo
Bina Mishra
Raj Kumar Singh
Bishnu Prasad Mishra
Ravi Kumar Gandham
author_facet Sajad Ahmad Wani
Manas Ranjan Praharaj
Amit R. Sahu
Raja Ishaq Nabi Khan
Shikha Saxena
Kaushal Kishor Rajak
Dhanavelu Muthuchelvan
Aditya Sahoo
Bina Mishra
Raj Kumar Singh
Bishnu Prasad Mishra
Ravi Kumar Gandham
author_sort Sajad Ahmad Wani
title Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
title_short Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
title_full Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
title_fullStr Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
title_full_unstemmed Systems Biology behind Immunoprotection of Both Sheep and Goats after Sungri/96 PPRV Vaccination
title_sort systems biology behind immunoprotection of both sheep and goats after sungri/96 pprv vaccination
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/39bb349a83994aa887bf309b22dbd075
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