Quantitative Proteomics Analysis of Lytic KSHV Infection in Human Endothelial Cells Reveals Targets of Viral Immune Modulation

Kaposi’s sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral rep...

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Published inCell reports (Cambridge) Vol. 33; no. 2; p. 108249
Main Authors Gabaev, Ildar, Williamson, James C., Crozier, Thomas W.M., Schulz, Thomas F., Lehner, Paul J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 13.10.2020
Cell Press
Subjects
Antigens, Differentiation, T-Lymphocyte - metabolism
Cell Line
DNA-Directed DNA Polymerase - metabolism
Down-Regulation
eIF-2 Kinase - metabolism
Endothelial Cells - immunology
Endothelial Cells - virology
Gene Library
Gene Ontology
Genes, Viral
Genetic Testing
herpesvirus
Herpesvirus 8, Human - genetics
Herpesvirus 8, Human - physiology
HHV-8
host cell restriction factors
Humans
Immunomodulation
Kinetics
KSHV
Ligands
lytic reactivation
Mutation - genetics
NK cell receptor ligands
Proteome - metabolism
Proteomics
Resource
Sarcoma, Kaposi - immunology
Sarcoma, Kaposi - virology
T Lineage-Specific Activation Antigen 1
Up-Regulation
viral immune evasion
Viral Proteins - metabolism
Virus Activation
proteomics
KSHV
herpesvirus
NK cell receptor ligands
HHV-8
lytic reactivation
viral immune evasion
host cell restriction factors
Online AccessGet full text
ISSN2211-1247
2211-1247
DOI10.1016/j.celrep.2020.108249

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Abstract Kaposi’s sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor. [Display omitted] •Quantitative proteomics identifies changes in host proteins induced by lytic KSHV•Targeting KSHV with CRISPR identifies CD155 and Nectin-2 as KSHV K5 substrates•Lytic KSHV downregulates protein kinase R in human endothelial cells•Kinetic profiling of lytic KSHV unravels PAA-sensitive and ORF57-dependent proteins Gabaev et al. describe how a human oncogenic herpesvirus, KSHV, changes the proteome of endothelial cells and modulates the host immune system. By targeting KSHV with CRISPR, they show that viral K5 protein downregulates ligands for the NK cell DNAM-1 receptor and antiviral protein PKR is depleted in an K5-independent manner.
AbstractList Kaposi's sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor.Kaposi's sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor.
Kaposi's sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor.
Kaposi’s sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor. • Quantitative proteomics identifies changes in host proteins induced by lytic KSHV • Targeting KSHV with CRISPR identifies CD155 and Nectin-2 as KSHV K5 substrates • Lytic KSHV downregulates protein kinase R in human endothelial cells • Kinetic profiling of lytic KSHV unravels PAA-sensitive and ORF57-dependent proteins Gabaev et al. describe how a human oncogenic herpesvirus, KSHV, changes the proteome of endothelial cells and modulates the host immune system. By targeting KSHV with CRISPR, they show that viral K5 protein downregulates ligands for the NK cell DNAM-1 receptor and antiviral protein PKR is depleted in an K5-independent manner.
Kaposi’s sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to lytic-stage infection initiates a cascade of viral gene expression. Here we show how these changes remodel the host cell proteome to enable viral replication. By undertaking a systematic and unbiased analysis of changes to the endothelial cell proteome following KSHV reactivation, we quantify >7,000 cellular proteins and 71 viral proteins and provide a temporal profile of protein changes during the course of lytic KSHV infection. Lytic KSHV induces >2-fold downregulation of 291 cellular proteins, including PKR, the key cellular sensor of double-stranded RNA. Despite the multiple episomes per cell, CRISPR-Cas9 efficiently targets KSHV genomes. A complementary KSHV genome-wide CRISPR genetic screen identifies K5 as the viral gene responsible for the downregulation of two KSHV targets, Nectin-2 and CD155, ligands of the NK cell DNAM-1 receptor. [Display omitted] •Quantitative proteomics identifies changes in host proteins induced by lytic KSHV•Targeting KSHV with CRISPR identifies CD155 and Nectin-2 as KSHV K5 substrates•Lytic KSHV downregulates protein kinase R in human endothelial cells•Kinetic profiling of lytic KSHV unravels PAA-sensitive and ORF57-dependent proteins Gabaev et al. describe how a human oncogenic herpesvirus, KSHV, changes the proteome of endothelial cells and modulates the host immune system. By targeting KSHV with CRISPR, they show that viral K5 protein downregulates ligands for the NK cell DNAM-1 receptor and antiviral protein PKR is depleted in an K5-independent manner.
ArticleNumber 108249
Author Gabaev, Ildar
Lehner, Paul J.
Williamson, James C.
Schulz, Thomas F.
Crozier, Thomas W.M.
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  organization: Department of Medicine, University of Cambridge, Hills Road, Cambridge CB2 0QQ, UK
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Issue 2
Keywords proteomics
KSHV
herpesvirus
NK cell receptor ligands
HHV-8
lytic reactivation
viral immune evasion
host cell restriction factors
Language English
License This is an open access article under the CC BY license.
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  doi: 10.1371/journal.ppat.1000334
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Snippet Kaposi’s sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to...
Kaposi's sarcoma herpesvirus (KSHV) is an oncogenic human virus and the leading cause of mortality in HIV infection. KSHV reactivation from latent- to...
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StartPage 108249
SubjectTerms Antigens, Differentiation, T-Lymphocyte - metabolism
Cell Line
DNA-Directed DNA Polymerase - metabolism
Down-Regulation
eIF-2 Kinase - metabolism
Endothelial Cells - immunology
Endothelial Cells - virology
Gene Library
Gene Ontology
Genes, Viral
Genetic Testing
herpesvirus
Herpesvirus 8, Human - genetics
Herpesvirus 8, Human - physiology
HHV-8
host cell restriction factors
Humans
Immunomodulation
Kinetics
KSHV
Ligands
lytic reactivation
Mutation - genetics
NK cell receptor ligands
Proteome - metabolism
Proteomics
Resource
Sarcoma, Kaposi - immunology
Sarcoma, Kaposi - virology
T Lineage-Specific Activation Antigen 1
Up-Regulation
viral immune evasion
Viral Proteins - metabolism
Virus Activation
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Title Quantitative Proteomics Analysis of Lytic KSHV Infection in Human Endothelial Cells Reveals Targets of Viral Immune Modulation
URI https://dx.doi.org/10.1016/j.celrep.2020.108249
https://www.ncbi.nlm.nih.gov/pubmed/33053346
https://www.proquest.com/docview/2451380322
https://pubmed.ncbi.nlm.nih.gov/PMC7567700
Volume 33
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