Shed GP of Ebola Virus Triggers Immune Activation and Increased Vascular Permeability
During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the bl...
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| Veröffentlicht in: | PLoS pathogens Jg. 10; H. 11; S. e1004509 |
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| Hauptverfasser: | , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
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United States
Public Library of Science
01.11.2014
Public Library of Science (PLoS) |
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| ISSN: | 1553-7374, 1553-7366, 1553-7374 |
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| Abstract | During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. |
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| AbstractList | During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. Ebola virus, a member of the Filoviridae family, causes lethal hemorrhagic fever in man and primates, displaying up to 90% mortality rates. Viral infection is typified by an excessive systemic inflammatory response resembling septic shock. It also damages endothelial cells and creates difficulty in coagulation, ultimately leading to haemorrhaging, organ failure and death. A unique feature of EBOV is that following infection high amounts of truncated surface GP, named shed GP, are released from infected cells and are detected in the blood of patients and experimentally infected animals. However the role of shed GP in virus replication and pathogenicity is not yet clearly defined. Here we show that shed GP released from virus-infected cells binds and activates non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and also affects vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity.During Ebola virus (EBOV) infection a significant amount of surface glycoprotein GP is shed from infected cells in a soluble form due to cleavage by cellular metalloprotease TACE. Shed GP and non-structural secreted glycoprotein sGP, both expressed from the same GP gene, have been detected in the blood of human patients and experimentally infected animals. In this study we demonstrate that shed GP could play a particular role during EBOV infection. In effect it binds and activates non-infected dendritic cells and macrophages inducing the secretion of pro- and anti-inflammatory cytokines (TNFα, IL1β, IL6, IL8, IL12p40, and IL1-RA, IL10). Activation of these cells by shed GP correlates with the increase in surface expression of co-stimulatory molecules CD40, CD80, CD83 and CD86. Contrary to shed GP, secreted sGP activates neither DC nor macrophages while it could bind DCs. In this study, we show that shed GP activity is likely mediated through cellular toll-like receptor 4 (TLR4) and is dependent on GP glycosylation. Treatment of cells with anti-TLR4 antibody completely abolishes shed GP-induced activation of cells. We also demonstrate that shed GP activity is negated upon addition of mannose-binding sera lectin MBL, a molecule known to interact with sugar arrays present on the surface of different microorganisms. Furthermore, we highlight the ability of shed GP to affect endothelial cell function both directly and indirectly, demonstrating the interplay between shed GP, systemic cytokine release and increased vascular permeability. In conclusion, shed GP released from virus-infected cells could activate non-infected DCs and macrophages causing the massive release of pro- and anti-inflammatory cytokines and effect vascular permeability. These activities could be at the heart of the excessive and dysregulated inflammatory host reactions to infection and thus contribute to high virus pathogenicity. |
| Audience | Academic |
| Author | Volchkova, Valentina A. Dolnik, Olga Escudero-Pérez, Beatriz Volchkov, Viktor E. Lawrence, Philip |
| AuthorAffiliation | Molecular Basis of Viral Pathogenicity, CIRI, INSERM U1111- CNRS UMR5308, Université de Lyon, Université Claude Bernard Lyon 1, Ecole Normale Supérieure de Lyon, Lyon, France Division of Clinical Research, United States of America |
| AuthorAffiliation_xml | – name: Division of Clinical Research, United States of America – name: Molecular Basis of Viral Pathogenicity, CIRI, INSERM U1111- CNRS UMR5308, Université de Lyon, Université Claude Bernard Lyon 1, Ecole Normale Supérieure de Lyon, Lyon, France |
| Author_xml | – sequence: 1 givenname: Beatriz surname: Escudero-Pérez fullname: Escudero-Pérez, Beatriz – sequence: 2 givenname: Valentina A. surname: Volchkova fullname: Volchkova, Valentina A. – sequence: 3 givenname: Olga surname: Dolnik fullname: Dolnik, Olga – sequence: 4 givenname: Philip surname: Lawrence fullname: Lawrence, Philip – sequence: 5 givenname: Viktor E. surname: Volchkov fullname: Volchkov, Viktor E. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25412102$$D View this record in MEDLINE/PubMed https://hal.science/hal-01911315$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2014 Public Library of Science Distributed under a Creative Commons Attribution 4.0 International License 2014 Escudero-Pérez et al 2014 Escudero-Pérez et al 2014 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: Escudero-Pérez B, Volchkova VA, Dolnik O, Lawrence P, Volchkov VE (2014) Shed GP of Ebola Virus Triggers Immune Activation and Increased Vascular Permeability. PLoS Pathog 10(11): e1004509. doi:10.1371/journal.ppat.1004509 |
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| Keywords | Human Umbilical Vein Endothelial Cells Ebolavirus Antigens CD Hemorrhagic Fever Dendritic Cells Guinea Pigs Toll-Like Receptor 4 Cytokines Humans Viral Proteins Macrophages Animals Membrane Glycoproteins Ebola |
| Language | English |
| License | Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 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 properly credited. Creative Commons Attribution License |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c733t-2af4c27a2f05d00b9723fd2d89bc83b851f3432b1f2f0ff823a2da367ff0751b3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC4239094 Conceived and designed the experiments: BEP VAV OD VEV. Performed the experiments: BEP VAV OD PL. Analyzed the data: BEP VAV VEV PL. Contributed reagents/materials/analysis tools: BEP VAV PL VEV. Wrote the paper: BEP PL VEV. The authors have declared that no competing interests exist. |
| ORCID | 0000-0002-7637-045X 0000-0003-3655-0525 0000-0001-7896-8706 |
| OpenAccessLink | https://doaj.org/article/ffe2e0b441fa45c6bc54f04f94c742bd |
| PMID | 25412102 |
| PQID | 1627073272 |
| PQPubID | 23479 |
| ParticipantIDs | plos_journals_1685290549 doaj_primary_oai_doaj_org_article_ffe2e0b441fa45c6bc54f04f94c742bd pubmedcentral_primary_oai_pubmedcentral_nih_gov_4239094 hal_primary_oai_HAL_hal_01911315v1 proquest_miscellaneous_1627073272 gale_infotracmisc_A393518095 gale_infotracacademiconefile_A393518095 gale_incontextgauss_ISR_A393518095 gale_incontextgauss_ISN_A393518095 pubmed_primary_25412102 crossref_primary_10_1371_journal_ppat_1004509 crossref_citationtrail_10_1371_journal_ppat_1004509 |
| PublicationCentury | 2000 |
| PublicationDate | 2014-11-01 |
| PublicationDateYYYYMMDD | 2014-11-01 |
| PublicationDate_xml | – month: 11 year: 2014 text: 2014-11-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco, USA |
| PublicationTitle | PLoS pathogens |
| PublicationTitleAlternate | PLoS Pathog |
| PublicationYear | 2014 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
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| SubjectTerms | Animals Antigens, CD - immunology Bacteriology Biology and Life Sciences Cytokines Cytokines - immunology Dendritic Cells - immunology Dendritic Cells - pathology Dendritic Cells - virology Ebola virus Ebolavirus - immunology Experiments Flow cytometry Guinea Pigs Health aspects Hemorrhagic Fever, Ebola - immunology Host-virus relationships Human Umbilical Vein Endothelial Cells - immunology Human Umbilical Vein Endothelial Cells - pathology Human Umbilical Vein Endothelial Cells - virology Humans Immune response Immune system Immunological research Immunology Infections Life Sciences Lymphocytes Macrophages - immunology Macrophages - pathology Macrophages - virology Medicine and Health Sciences Membrane Glycoproteins - immunology Microbiology and Parasitology Mortality Permeability Statistical analysis Toll-Like Receptor 4 - immunology Viral infections Viral Proteins - immunology Virology Virus research |
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| Title | Shed GP of Ebola Virus Triggers Immune Activation and Increased Vascular Permeability |
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