Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection

Marek’s disease virus (MDV), an alpha herpes virus, causes a lymphoproliferative state in chickens known as Marek’s disease (MD), resulting in severe monetary losses to the poultry industry. Because lymphocytes of bursa of Fabricius and spleen are prime targets of MDV replication...

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Main Authors: Huan Jin, Zimeng Kong, Arslan Mehboob, Bo Jiang, Jian Xu, Yunhong Cai, Wenxiao Liu, Jiabing Hong, Yongqing Li
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/12/3/354
id doaj-2c075bbc5afe46beb33f9bd0f743689a
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Huan Jin
Zimeng Kong
Arslan Mehboob
Bo Jiang
Jian Xu
Yunhong Cai
Wenxiao Liu
Jiabing Hong
Yongqing Li
spellingShingle Huan Jin
Zimeng Kong
Arslan Mehboob
Bo Jiang
Jian Xu
Yunhong Cai
Wenxiao Liu
Jiabing Hong
Yongqing Li
Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
Viruses
marek’s disease virus
lymphocytes
differentially expressed genes
cytokine
chemokine
author_facet Huan Jin
Zimeng Kong
Arslan Mehboob
Bo Jiang
Jian Xu
Yunhong Cai
Wenxiao Liu
Jiabing Hong
Yongqing Li
author_sort Huan Jin
title Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
title_short Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
title_full Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
title_fullStr Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
title_full_unstemmed Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic Infection
title_sort transcriptional profiles associated with marek’s disease virus in bursa and spleen lymphocytes reveal contrasting immune responses during early cytolytic infection
publisher MDPI AG
series Viruses
issn 1999-4915
publishDate 2020-03-01
description Marek’s disease virus (MDV), an alpha herpes virus, causes a lymphoproliferative state in chickens known as Marek’s disease (MD), resulting in severe monetary losses to the poultry industry. Because lymphocytes of bursa of Fabricius and spleen are prime targets of MDV replication during the early cytolytic phase of infection, the immune response in bursa and spleen should be the foundation of late immunity induced by MDV. However, the mechanism of the MDV-mediated host immune response in lymphocytes in the early stage is poorly understood. The present study is primarily aimed at identifying the crucial genes and significant pathways involved in the immune response of chickens infected with MDV CVI988 and the very virulent RB1B (vvRB1B) strains. Using the RNA sequencing approach, we analyzed the generated transcriptomes from lymphocytes isolated from chicken bursa and spleen. Our findings validated the expression of previously characterized genes; however, they also revealed the expression of novel genes during the MDV-mediated immune response. The results showed that after challenge with CVI988 or vvRB1B strains, 634 and 313 differentially expressed genes (DEGs) were identified in splenic lymphocytes, respectively. However, 58 and 47 DEGs were observed in bursal lymphocytes infected with CVI988 and vvRB1B strains, respectively. Following MDV CVI988 or vvRB1B challenge, the bursal lymphocytes displayed changes in IL-6 and IL-4 gene expression. Surprisingly, splenic lymphocytes exhibited an overwhelming alteration in the expression of cytokines and cytokine receptors involved in immune response signaling. On the other hand, there was no distinct trend between infection with CVI988 and vvRB1B and the expression of cytokines and chemokines, such as IL-10, IFN-γ, STAT1, IRF1, CCL19, and CCL26. However, the expression profiles of IL-1β, IL-6, IL8L1, CCL4 (GGCL1), and CCL5 were significantly upregulated in splenic lymphocytes from chickens infected with CVI988 compared with those of chickens infected with vvRB1B. Because these cytokines and chemokines are considered to be associated with B cell activation and antigenic signal transduction to T cells, they may indicate differences of immune responses initiated by vaccinal and virulent strains during the early phase of infection. Collectively, our study provides valuable data on the transcriptional landscape using high-throughput sequencing to understand the different mechanism between vaccine-mediated protection and pathogenesis of virulent MDV in vivo.
topic marek’s disease virus
lymphocytes
differentially expressed genes
cytokine
chemokine
url https://www.mdpi.com/1999-4915/12/3/354
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spelling doaj-2c075bbc5afe46beb33f9bd0f743689a2020-11-25T01:28:23ZengMDPI AGViruses1999-49152020-03-0112335410.3390/v12030354v12030354Transcriptional Profiles Associated with Marek’s Disease Virus in Bursa and Spleen Lymphocytes Reveal Contrasting Immune Responses during Early Cytolytic InfectionHuan Jin0Zimeng Kong1Arslan Mehboob2Bo Jiang3Jian Xu4Yunhong Cai5Wenxiao Liu6Jiabing Hong7Yongqing Li8Research Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaResearch Center for Infectious Disease in Livestock and Poultry, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, ChinaMarek’s disease virus (MDV), an alpha herpes virus, causes a lymphoproliferative state in chickens known as Marek’s disease (MD), resulting in severe monetary losses to the poultry industry. Because lymphocytes of bursa of Fabricius and spleen are prime targets of MDV replication during the early cytolytic phase of infection, the immune response in bursa and spleen should be the foundation of late immunity induced by MDV. However, the mechanism of the MDV-mediated host immune response in lymphocytes in the early stage is poorly understood. The present study is primarily aimed at identifying the crucial genes and significant pathways involved in the immune response of chickens infected with MDV CVI988 and the very virulent RB1B (vvRB1B) strains. Using the RNA sequencing approach, we analyzed the generated transcriptomes from lymphocytes isolated from chicken bursa and spleen. Our findings validated the expression of previously characterized genes; however, they also revealed the expression of novel genes during the MDV-mediated immune response. The results showed that after challenge with CVI988 or vvRB1B strains, 634 and 313 differentially expressed genes (DEGs) were identified in splenic lymphocytes, respectively. However, 58 and 47 DEGs were observed in bursal lymphocytes infected with CVI988 and vvRB1B strains, respectively. Following MDV CVI988 or vvRB1B challenge, the bursal lymphocytes displayed changes in IL-6 and IL-4 gene expression. Surprisingly, splenic lymphocytes exhibited an overwhelming alteration in the expression of cytokines and cytokine receptors involved in immune response signaling. On the other hand, there was no distinct trend between infection with CVI988 and vvRB1B and the expression of cytokines and chemokines, such as IL-10, IFN-γ, STAT1, IRF1, CCL19, and CCL26. However, the expression profiles of IL-1β, IL-6, IL8L1, CCL4 (GGCL1), and CCL5 were significantly upregulated in splenic lymphocytes from chickens infected with CVI988 compared with those of chickens infected with vvRB1B. Because these cytokines and chemokines are considered to be associated with B cell activation and antigenic signal transduction to T cells, they may indicate differences of immune responses initiated by vaccinal and virulent strains during the early phase of infection. Collectively, our study provides valuable data on the transcriptional landscape using high-throughput sequencing to understand the different mechanism between vaccine-mediated protection and pathogenesis of virulent MDV in vivo.https://www.mdpi.com/1999-4915/12/3/354marek’s disease viruslymphocytesdifferentially expressed genescytokinechemokine