Single-cell profiling of African swine fever virus disease in the pig spleen reveals viral and host dynamics

African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the c...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 121; no. 10; p. e2312150121
Main Authors Zhu, Zixiang, Mao, Ruoqing, Liu, Baohong, Liu, Huanan, Shi, Zhengwang, Zhang, Kunpeng, Liu, Huisheng, Zhang, Danyang, Liu, Jia, Zhao, Zhenxiang, Li, Kangli, Yang, Fan, Cao, Weijun, Zhang, Xiangle, Shen, Chaochao, Sun, Dehui, Wang, Liyuan, Tian, Hong, Ru, Yi, Feng, Tao, He, Jijun, Guo, Jianhong, Zhang, Keshan, Tang, Zhonglin, Zhang, Shilei, Ding, Chan, Han, Jun, Zheng, Haixue
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 05.03.2024
Subjects
African swine fever
Antigen presentation
Apoptosis
Asfarviridae
Biological Sciences
CD14 antigen
Fever
Gene sequencing
Heterogeneity
Hogs
Immune response
In vivo methods and tests
Infections
Macrophages
Monocytes
Organs
Replication
Spleen
Swine
Tropism
Viral diseases
Viral infections
Viruses
host antiviral response
single-cell RNA sequencing
monocytes
African swine fever virus
cellular tropism
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Abstract African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the cell population to drive high-efficient replication of the virus in vivo remains unclear. Here, we found that the spleen reveals the most severe pathological manifestation with the highest viral loads among various organs in pigs during ASFV infection. By using single-cell-RNA-sequencing technology and multiple methods, we determined that macrophages and monocytes are the major cell types infected by ASFV in the spleen, showing high viral-load heterogeneity. A rare subpopulation of immature monocytes represents the major population infected at late infection stage. ASFV causes massive death of macrophages, but shifts its infection into these monocytes which significantly arise after the infection. The apoptosis, interferon response, and antigen-presentation capacity are inhibited in these monocytes which benefits prolonged infection of ASFV in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked due to that they do not express classical monocyte marker CD14. The present study indicates that the shift of viral infection from macrophages to the immature monocytes is critical for maintaining prolonged ASFV infection in vivo. This study sheds light on ASFV tropism, replication, and infection dynamics, and elicited immune response, which may instruct future research on antiviral strategies.
AbstractList African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the cell population to drive high-efficient replication of the virus in vivo remains unclear. Here, we found that the spleen reveals the most severe pathological manifestation with the highest viral loads among various organs in pigs during ASFV infection. By using single-cell-RNA-sequencing technology and multiple methods, we determined that macrophages and monocytes are the major cell types infected by ASFV in the spleen, showing high viral-load heterogeneity. A rare subpopulation of immature monocytes represents the major population infected at late infection stage. ASFV causes massive death of macrophages, but shifts its infection into these monocytes which significantly arise after the infection. The apoptosis, interferon response, and antigen-presentation capacity are inhibited in these monocytes which benefits prolonged infection of ASFV in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked due to that they do not express classical monocyte marker CD14. The present study indicates that the shift of viral infection from macrophages to the immature monocytes is critical for maintaining prolonged ASFV infection in vivo. This study sheds light on ASFV tropism, replication, and infection dynamics, and elicited immune response, which may instruct future research on antiviral strategies.
African swine fever is arguably the most severe infectious disease threating the global pig industry. However, how African swine fever virus (ASFV) manipulates the infected cell population and controls host responses to drive high-efficient replication of the virus in vivo remains unclear. Our work suggested that the shift of ASFV infection from macrophages to an unusual subpopulation of immature monocytes and insufficient antiviral responses drive prolonged infection in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked. We identified molecular determinants of tropism and examined temporal dynamics in viral and host gene expression in these cells, which will help in rationale design of antivirals or vaccines and clarify ASFV pathogenesis. African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the cell population to drive high-efficient replication of the virus in vivo remains unclear. Here, we found that the spleen reveals the most severe pathological manifestation with the highest viral loads among various organs in pigs during ASFV infection. By using single-cell-RNA-sequencing technology and multiple methods, we determined that macrophages and monocytes are the major cell types infected by ASFV in the spleen, showing high viral-load heterogeneity. A rare subpopulation of immature monocytes represents the major population infected at late infection stage. ASFV causes massive death of macrophages, but shifts its infection into these monocytes which significantly arise after the infection. The apoptosis, interferon response, and antigen-presentation capacity are inhibited in these monocytes which benefits prolonged infection of ASFV in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked due to that they do not express classical monocyte marker CD14. The present study indicates that the shift of viral infection from macrophages to the immature monocytes is critical for maintaining prolonged ASFV infection in vivo. This study sheds light on ASFV tropism, replication, and infection dynamics, and elicited immune response, which may instruct future research on antiviral strategies.
African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the cell population to drive high-efficient replication of the virus in vivo remains unclear. Here, we found that the spleen reveals the most severe pathological manifestation with the highest viral loads among various organs in pigs during ASFV infection. By using single-cell-RNA-sequencing technology and multiple methods, we determined that macrophages and monocytes are the major cell types infected by ASFV in the spleen, showing high viral-load heterogeneity. A rare subpopulation of immature monocytes represents the major population infected at late infection stage. ASFV causes massive death of macrophages, but shifts its infection into these monocytes which significantly arise after the infection. The apoptosis, interferon response, and antigen-presentation capacity are inhibited in these monocytes which benefits prolonged infection of ASFV in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked due to that they do not express classical monocyte marker CD14. The present study indicates that the shift of viral infection from macrophages to the immature monocytes is critical for maintaining prolonged ASFV infection in vivo. This study sheds light on ASFV tropism, replication, and infection dynamics, and elicited immune response, which may instruct future research on antiviral strategies.African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the causative agent African swine fever virus (ASFV) in various organs in pigs greatly contributes to the disease. However, how ASFV manipulates the cell population to drive high-efficient replication of the virus in vivo remains unclear. Here, we found that the spleen reveals the most severe pathological manifestation with the highest viral loads among various organs in pigs during ASFV infection. By using single-cell-RNA-sequencing technology and multiple methods, we determined that macrophages and monocytes are the major cell types infected by ASFV in the spleen, showing high viral-load heterogeneity. A rare subpopulation of immature monocytes represents the major population infected at late infection stage. ASFV causes massive death of macrophages, but shifts its infection into these monocytes which significantly arise after the infection. The apoptosis, interferon response, and antigen-presentation capacity are inhibited in these monocytes which benefits prolonged infection of ASFV in vivo. Until now, the role of immature monocytes as an important target by ASFV has been overlooked due to that they do not express classical monocyte marker CD14. The present study indicates that the shift of viral infection from macrophages to the immature monocytes is critical for maintaining prolonged ASFV infection in vivo. This study sheds light on ASFV tropism, replication, and infection dynamics, and elicited immune response, which may instruct future research on antiviral strategies.
Author Cao, Weijun
Zhang, Danyang
Zhao, Zhenxiang
Zhang, Kunpeng
Guo, Jianhong
Zhang, Keshan
Liu, Huisheng
Feng, Tao
He, Jijun
Han, Jun
Liu, Jia
Li, Kangli
Zhu, Zixiang
Mao, Ruoqing
Sun, Dehui
Ding, Chan
Shen, Chaochao
Zheng, Haixue
Liu, Huanan
Tian, Hong
Ru, Yi
Liu, Baohong
Yang, Fan
Wang, Liyuan
Shi, Zhengwang
Zhang, Xiangle
Tang, Zhonglin
Zhang, Shilei
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Keywords host antiviral response
single-cell RNA sequencing
monocytes
African swine fever virus
cellular tropism
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Edited by Xiang-Jin Meng, Virginia Polytechnic Institute and State University, Blacksburg, VA; received July 22, 2023; accepted January 8, 2024
1Z. Zhu, R.M., and B.L. contributed equally to this work.
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Snippet African swine fever, one of the major viral diseases of swine, poses an imminent threat to the global pig industry. The high-efficient replication of the...
African swine fever is arguably the most severe infectious disease threating the global pig industry. However, how African swine fever virus (ASFV) manipulates...
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SourceType Open Access Repository
Aggregation Database
Index Database
StartPage e2312150121
SubjectTerms African swine fever
Antigen presentation
Apoptosis
Asfarviridae
Biological Sciences
CD14 antigen
Fever
Gene sequencing
Heterogeneity
Hogs
Immune response
In vivo methods and tests
Infections
Macrophages
Monocytes
Organs
Replication
Spleen
Swine
Tropism
Viral diseases
Viral infections
Viruses
Title Single-cell profiling of African swine fever virus disease in the pig spleen reveals viral and host dynamics
URI https://www.ncbi.nlm.nih.gov/pubmed/38412127
https://www.proquest.com/docview/2954293043
https://www.proquest.com/docview/2932937450/abstract/
https://pubmed.ncbi.nlm.nih.gov/PMC10927503
Volume 121
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