Single-nucleus sequencing of silkworm larval midgut reveals the immune escape strategy of BmNPV in the midgut during the late stage of infection

The midgut is an important barrier against microorganism invasion and proliferation, yet is the first tissue encountered when a baculovirus naturally invades the host. However, only limited knowledge is available how different midgut cell types contribute to the immune response and the clearance or...

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Published inInsect biochemistry and molecular biology Vol. 164; p. 104043
Main Authors Xia, Junming, Fei, Shigang, Huang, Yigui, Lai, Wenxuan, Yu, Yue, Liang, Lingying, Wu, Hailin, Swevers, Luc, Sun, Jingchen, Feng, Min
Format Journal Article
LanguageEnglish
Published England 01.01.2024
Subjects
Animals
Antiviral Agents
Bombyx - genetics
Bombyx - metabolism
Digestive System
Larva - metabolism
Nucleopolyhedroviruses - metabolism
Single-nucleus RNA sequencing
Baculovirus
Midgut
BmNPV
Silkworm
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Abstract The midgut is an important barrier against microorganism invasion and proliferation, yet is the first tissue encountered when a baculovirus naturally invades the host. However, only limited knowledge is available how different midgut cell types contribute to the immune response and the clearance or promotion of viral infection. Here, single-nucleus RNA sequencing (snRNA seq) was employed to analyze the responses of various cell subpopulations in the silkworm larval midgut to B. mori nucleopolyhedrovirus (BmNPV) infection. We identified 22 distinct clusters representing enteroendocrine cells (EEs), enterocytes (ECs), intestinal stem cells (ISCs), Goblet cell-like and muscle cell types in the BmNPV-infected and uninfected silkworm larvae midgut at 72 h post infection. Further, our results revealed that the strategies for immune escape of BmNPV in the midgut at the late stage of infection include (1) inhibiting the response of antiviral pathways; (2) inhibiting the expression of antiviral host factors; (3) stimulating expression levels of genes promoting BmNPV replication. These findings suggest that the midgut, as the first line of defense against the invasion of the baculovirus, has dual characteristics of "resistance" and "tolerance". Our single-cell dataset reveals the diversity of silkworm larval midgut cells, and the transcriptome analysis provides insights into the interaction between host and virus infection at the single-cell level.
AbstractList The midgut is an important barrier against microorganism invasion and proliferation, yet is the first tissue encountered when a baculovirus naturally invades the host. However, only limited knowledge is available how different midgut cell types contribute to the immune response and the clearance or promotion of viral infection. Here, single-nucleus RNA sequencing (snRNA seq) was employed to analyze the responses of various cell subpopulations in the silkworm larval midgut to B. mori nucleopolyhedrovirus (BmNPV) infection. We identified 22 distinct clusters representing enteroendocrine cells (EEs), enterocytes (ECs), intestinal stem cells (ISCs), Goblet cell-like and muscle cell types in the BmNPV-infected and uninfected silkworm larvae midgut at 72 h post infection. Further, our results revealed that the strategies for immune escape of BmNPV in the midgut at the late stage of infection include (1) inhibiting the response of antiviral pathways; (2) inhibiting the expression of antiviral host factors; (3) stimulating expression levels of genes promoting BmNPV replication. These findings suggest that the midgut, as the first line of defense against the invasion of the baculovirus, has dual characteristics of "resistance" and "tolerance". Our single-cell dataset reveals the diversity of silkworm larval midgut cells, and the transcriptome analysis provides insights into the interaction between host and virus infection at the single-cell level.
The midgut is an important barrier against microorganism invasion and proliferation, yet is the first tissue encountered when a baculovirus naturally invades the host. However, only limited knowledge is available how different midgut cell types contribute to the immune response and the clearance or promotion of viral infection. Here, single-nucleus RNA sequencing (snRNA seq) was employed to analyze the responses of various cell subpopulations in the silkworm larval midgut to B. mori nucleopolyhedrovirus (BmNPV) infection. We identified 22 distinct clusters representing enteroendocrine cells (EEs), enterocytes (ECs), intestinal stem cells (ISCs), Goblet cell-like and muscle cell types in the BmNPV-infected and uninfected silkworm larvae midgut at 72 h post infection. Further, our results revealed that the strategies for immune escape of BmNPV in the midgut at the late stage of infection include (1) inhibiting the response of antiviral pathways; (2) inhibiting the expression of antiviral host factors; (3) stimulating expression levels of genes promoting BmNPV replication. These findings suggest that the midgut, as the first line of defense against the invasion of the baculovirus, has dual characteristics of "resistance" and "tolerance". Our single-cell dataset reveals the diversity of silkworm larval midgut cells, and the transcriptome analysis provides insights into the interaction between host and virus infection at the single-cell level.
ArticleNumber 104043
Author Fei, Shigang
Xia, Junming
Yu, Yue
Sun, Jingchen
Liang, Lingying
Swevers, Luc
Lai, Wenxuan
Huang, Yigui
Wu, Hailin
Feng, Min
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  surname: Xia
  fullname: Xia, Junming
  email: xiajm2018@163.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: xiajm2018@163.com
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  surname: Huang
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  email: wardrobe23@163.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: wardrobe23@163.com
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  givenname: Wenxuan
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  fullname: Lai, Wenxuan
  email: zczx120604@126.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: zczx120604@126.com
– sequence: 5
  givenname: Yue
  surname: Yu
  fullname: Yu, Yue
  email: yy616230739@163.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: yy616230739@163.com
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  surname: Liang
  fullname: Liang, Lingying
  email: 13656892183@163.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: 13656892183@163.com
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  givenname: Hailin
  surname: Wu
  fullname: Wu, Hailin
  email: 18029116452@163.com
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: 18029116452@163.com
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  givenname: Luc
  surname: Swevers
  fullname: Swevers, Luc
  email: swevers@bio.demokritos.gr
  organization: Insect Molecular Genetics and Biotechnology, National Centre for Scientific Research Demokritos, Institute of Biosciences and Applications, Athens, Greece. Electronic address: swevers@bio.demokritos.gr
– sequence: 9
  givenname: Jingchen
  surname: Sun
  fullname: Sun, Jingchen
  email: cyfz@scau.edu.cn
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: cyfz@scau.edu.cn
– sequence: 10
  givenname: Min
  surname: Feng
  fullname: Feng, Min
  email: hunanfengmin@scau.edu.cn
  organization: Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, China. Electronic address: hunanfengmin@scau.edu.cn
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Keywords Single-nucleus RNA sequencing
Baculovirus
Midgut
BmNPV
Silkworm
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Snippet The midgut is an important barrier against microorganism invasion and proliferation, yet is the first tissue encountered when a baculovirus naturally invades...
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SubjectTerms Animals
Antiviral Agents
Bombyx - genetics
Bombyx - metabolism
Digestive System
Larva - metabolism
Nucleopolyhedroviruses - metabolism
Title Single-nucleus sequencing of silkworm larval midgut reveals the immune escape strategy of BmNPV in the midgut during the late stage of infection
URI https://www.ncbi.nlm.nih.gov/pubmed/38013005
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