Analysis of the SUMO2 Proteome during HSV-1 Infection

Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins are regulated. Sumoylation has roles in the control of protein stability, activity and localization, and is involved in the regulation of trans...

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Published inPLoS pathogens Vol. 11; no. 7; p. e1005059
Main Authors Sloan, Elizabeth, Tatham, Michael H, Groslambert, Marine, Glass, Mandy, Orr, Anne, Hay, Ronald T, Everett, Roger D
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.07.2015
Public Library of Science (PLoS)
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Abstract Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins are regulated. Sumoylation has roles in the control of protein stability, activity and localization, and is involved in the regulation of transcription, gene expression, chromatin structure, nuclear transport and RNA metabolism. Sumoylation is also linked, both positively and negatively, with the replication of many different viruses both in terms of modification of viral proteins and modulation of sumoylated cellular proteins that influence the efficiency of infection. One prominent example of the latter is the widespread reduction in the levels of cellular sumoylated species induced by herpes simplex virus type 1 (HSV-1) ubiquitin ligase ICP0. This activity correlates with relief from intrinsic immunity antiviral defence mechanisms. Previous work has shown that ICP0 is selective in substrate choice, with some sumoylated proteins such the promyelocytic leukemia protein PML being extremely sensitive, while RanGAP is completely resistant. Here we present a comprehensive proteomic analysis of changes in the cellular SUMO2 proteome during HSV-1 infection. Amongst the 877 potentially sumoylated species detected, we identified 124 whose abundance was decreased by a factor of 3 or more by the virus, several of which were validated by western blot and expression analysis. We found many previously undescribed substrates of ICP0 whose degradation occurs by a range of mechanisms, influenced or not by sumoylation and/or the SUMO2 interaction motif within ICP0. Many of these proteins are known or are predicted to be involved in the regulation of transcription, chromatin assembly or modification. These results present novel insights into mechanisms and host cell proteins that might influence the efficiency of HSV-1 infection.
AbstractList   Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins are regulated. Sumoylation has roles in the control of protein stability, activity and localization, and is involved in the regulation of transcription, gene expression, chromatin structure, nuclear transport and RNA metabolism. Sumoylation is also linked, both positively and negatively, with the replication of many different viruses both in terms of modification of viral proteins and modulation of sumoylated cellular proteins that influence the efficiency of infection. One prominent example of the latter is the widespread reduction in the levels of cellular sumoylated species induced by herpes simplex virus type 1 (HSV-1) ubiquitin ligase ICP0. This activity correlates with relief from intrinsic immunity antiviral defence mechanisms. Previous work has shown that ICP0 is selective in substrate choice, with some sumoylated proteins such the promyelocytic leukemia protein PML being extremely sensitive, while RanGAP is completely resistant. Here we present a comprehensive proteomic analysis of changes in the cellular SUMO2 proteome during HSV-1 infection. Amongst the 877 potentially sumoylated species detected, we identified 124 whose abundance was decreased by a factor of 3 or more by the virus, several of which were validated by western blot and expression analysis. We found many previously undescribed substrates of ICP0 whose degradation occurs by a range of mechanisms, influenced or not by sumoylation and/or the SUMO2 interaction motif within ICP0. Many of these proteins are known or are predicted to be involved in the regulation of transcription, chromatin assembly or modification. These results present novel insights into mechanisms and host cell proteins that might influence the efficiency of HSV-1 infection.
Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins are regulated. Sumoylation has roles in the control of protein stability, activity and localization, and is involved in the regulation of transcription, gene expression, chromatin structure, nuclear transport and RNA metabolism. Sumoylation is also linked, both positively and negatively, with the replication of many different viruses both in terms of modification of viral proteins and modulation of sumoylated cellular proteins that influence the efficiency of infection. One prominent example of the latter is the widespread reduction in the levels of cellular sumoylated species induced by herpes simplex virus type 1 (HSV-1) ubiquitin ligase ICP0. This activity correlates with relief from intrinsic immunity antiviral defence mechanisms. Previous work has shown that ICP0 is selective in substrate choice, with some sumoylated proteins such the promyelocytic leukemia protein PML being extremely sensitive, while RanGAP is completely resistant. Here we present a comprehensive proteomic analysis of changes in the cellular SUMO2 proteome during HSV-1 infection. Amongst the 877 potentially sumoylated species detected, we identified 124 whose abundance was decreased by a factor of 3 or more by the virus, several of which were validated by western blot and expression analysis. We found many previously undescribed substrates of ICP0 whose degradation occurs by a range of mechanisms, influenced or not by sumoylation and/or the SUMO2 interaction motif within ICP0. Many of these proteins are known or are predicted to be involved in the regulation of transcription, chromatin assembly or modification. These results present novel insights into mechanisms and host cell proteins that might influence the efficiency of HSV-1 infection.
Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins are regulated. Sumoylation has roles in the control of protein stability, activity and localization, and is involved in the regulation of transcription, gene expression, chromatin structure, nuclear transport and RNA metabolism. Sumoylation is also linked, both positively and negatively, with the replication of many different viruses both in terms of modification of viral proteins and modulation of sumoylated cellular proteins that influence the efficiency of infection. One prominent example of the latter is the widespread reduction in the levels of cellular sumoylated species induced by herpes simplex virus type 1 (HSV-1) ubiquitin ligase ICP0. This activity correlates with relief from intrinsic immunity antiviral defence mechanisms. Previous work has shown that ICP0 is selective in substrate choice, with some sumoylated proteins such the promyelocytic leukemia protein PML being extremely sensitive, while RanGAP is completely resistant. Here we present a comprehensive proteomic analysis of changes in the cellular SUMO2 proteome during HSV-1 infection. Amongst the 877 potentially sumoylated species detected, we identified 124 whose abundance was decreased by a factor of 3 or more by the virus, several of which were validated by western blot and expression analysis. We found many previously undescribed substrates of ICP0 whose degradation occurs by a range of mechanisms, influenced or not by sumoylation and/or the SUMO2 interaction motif within ICP0. Many of these proteins are known or are predicted to be involved in the regulation of transcription, chromatin assembly or modification. These results present novel insights into mechanisms and host cell proteins that might influence the efficiency of HSV-1 infection. Proteins are subject to many types of modification that regulate their functions and which are applied after their initial synthesis in the cell. One such modification is known as sumoylation, the covalent linkage of a small ubiquitin-like protein to a wide variety of substrate proteins. Sumoylation is involved in the regulation of many cellular pathways, including transcription, DNA repair, chromatin modification and defence to viral infections. Several viruses have connections with sumoylation, either through modification of their own proteins or in changing the sumoylation status of cellular proteins in ways that may be beneficial for infection. Herpes simplex virus type 1 (HSV-1) causes a widespread reduction in uncharacterized sumoylated cellular protein species, an effect that is caused by one of its key regulatory proteins (ICP0), which also induces the degradation of a number of repressive cellular proteins and thereby stimulates efficient infection. This study describes a comprehensive analysis of cellular proteins whose sumoylation status is altered by HSV-1 infection. Of 877 putative cellular sumoylation substrates, we found 124 whose sumoylation status reduces at least three-fold during infection. We validated the behavior of several such proteins and identified amongst them several novel targets of ICP0 activity with predicted repressive properties.
Author Hay, Ronald T
Orr, Anne
Everett, Roger D
Sloan, Elizabeth
Tatham, Michael H
Groslambert, Marine
Glass, Mandy
AuthorAffiliation 1 MRC-University of Glasgow Centre for Virus Research, The Sir Michael Stoker Building, University of Glasgow Garscube Campus, Glasgow, Scotland, United Kingdom
2 Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Dundee, United Kingdom
Baylor College of Medicine, UNITED STATES
AuthorAffiliation_xml – name: 2 Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Dundee, United Kingdom
– name: Baylor College of Medicine, UNITED STATES
– name: 1 MRC-University of Glasgow Centre for Virus Research, The Sir Michael Stoker Building, University of Glasgow Garscube Campus, Glasgow, Scotland, United Kingdom
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  organization: MRC-University of Glasgow Centre for Virus Research, The Sir Michael Stoker Building, University of Glasgow Garscube Campus, Glasgow, Scotland, United Kingdom
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  surname: Tatham
  fullname: Tatham, Michael H
  organization: Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Dundee, United Kingdom
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  surname: Groslambert
  fullname: Groslambert, Marine
  organization: MRC-University of Glasgow Centre for Virus Research, The Sir Michael Stoker Building, University of Glasgow Garscube Campus, Glasgow, Scotland, United Kingdom
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  givenname: Mandy
  surname: Glass
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  givenname: Roger D
  surname: Everett
  fullname: Everett, Roger D
  organization: MRC-University of Glasgow Centre for Virus Research, The Sir Michael Stoker Building, University of Glasgow Garscube Campus, Glasgow, Scotland, United Kingdom
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2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Sloan E, Tatham MH, Groslambert M, Glass M, Orr A, Hay RT, et al. (2015) Analysis of the SUMO2 Proteome during HSV-1 Infection. PLoS Pathog 11(7): e1005059. doi:10.1371/journal.ppat.1005059
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Conceived and designed the experiments: ES MHT MGr MGl RTH RDE. Performed the experiments: ES MHT MGr MGl AO. Analyzed the data: ES MHT MGr MGl RTH RDE. Contributed reagents/materials/analysis tools: ES MHT MGr MGl RTH RDE. Wrote the paper: ES MHT RDE.
Current address: Département de Biologie, Ecole Normale Supérieure de Lyon, Lyon, France
The authors have declared that no competing interests exist.
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Snippet Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins...
  Covalent linkage to members of the small ubiquitin-like (SUMO) family of proteins is an important mechanism by which the functions of many cellular proteins...
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StartPage e1005059
SubjectTerms Cell Line
Experiments
Gene expression
Gene Expression Regulation, Viral - genetics
Herpes viruses
Herpesvirus 1, Human
Host-Pathogen Interactions
Humans
Infections
Medical research
Proteins
Proteome - genetics
Proteome - metabolism
Proteomics - methods
Signal transduction
Small Ubiquitin-Related Modifier Proteins - genetics
Small Ubiquitin-Related Modifier Proteins - immunology
Small Ubiquitin-Related Modifier Proteins - metabolism
Transcription Factors - metabolism
Tumor Suppressor Proteins - metabolism
Viral infections
Viral Proteins - metabolism
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Title Analysis of the SUMO2 Proteome during HSV-1 Infection
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http://dx.doi.org/10.1371/journal.ppat.1005059
Volume 11
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