Endothelial Cells Support Persistent Gammaherpesvirus 68 Infection
Identifieur interne : 000A26 ( Pmc/Curation ); précédent : 000A25; suivant : 000A27Endothelial Cells Support Persistent Gammaherpesvirus 68 Infection
Auteurs : Andrea Luísa Suárez [États-Unis] ; Linda Faye Van Dyk [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2008.
Abstract
A variety of human diseases are associated with gammaherpesviruses, including neoplasms of lymphocytes (e.g. Burkitt's lymphoma) and endothelial cells (e.g. Kaposi's sarcoma). Gammaherpesvirus infections usually result in either a productive lytic infection, characterized by expression of all viral genes and rapid cell lysis, or latent infection, characterized by limited viral gene expression and no cell lysis. Here, we report characterization of endothelial cell infection with murine gammaherpesvirus 68 (γHV68), a virus phylogenetically related and biologically similar to the human gammaherpesviruses. Endothelial cells supported γHV68 replication
Url:
DOI: 10.1371/journal.ppat.1000152
PubMed: 18787698
PubMed Central: 2526176
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<wicri:regionArea>Department of Microbiology and Program in Molecular Biology, University of Colorado Denver School of Medicine, Aurora, Colorado</wicri:regionArea>
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<front><div type="abstract" xml:lang="en"><p>A variety of human diseases are associated with gammaherpesviruses, including neoplasms of lymphocytes (e.g. Burkitt's lymphoma) and endothelial cells (e.g. Kaposi's sarcoma). Gammaherpesvirus infections usually result in either a productive lytic infection, characterized by expression of all viral genes and rapid cell lysis, or latent infection, characterized by limited viral gene expression and no cell lysis. Here, we report characterization of endothelial cell infection with murine gammaherpesvirus 68 (γHV68), a virus phylogenetically related and biologically similar to the human gammaherpesviruses. Endothelial cells supported γHV68 replication <italic>in vitro</italic>
, but were unique in that a significant proportion of the cells escaped lysis, proliferated, and remained viable in culture for an extended time. Upon infection, endothelial cells became non-adherent and altered in size, complexity, and cell-surface protein expression. These cells were uniformly infected and expressed the lytic transcription program based on detection of abundant viral gene transcripts, GFP fluorescence from the viral genome, and viral surface protein expression. Additionally, endothelial cells continued to produce new infectious virions as late as 30 days post-infection. The outcome of this long-term infection was promoted by the γHV68 v-cyclin, because in the absence of the v-cyclin, viability was significantly reduced following infection. Importantly, infected primary endothelial cells also demonstrated increased viability relative to infected primary fibroblasts, and this increased viability was dependent on the v-cyclin. Finally, we provide evidence for infection of endothelial cells <italic>in vivo</italic>
in immune-deficient mice. The extended viability and virus production of infected endothelial cells indicated that endothelial cells provided a source of prolonged virus production and identify a cell-type specific adaptation of gammaherpesvirus replication. While infected endothelial cells would likely be cleared in a healthy individual, persistently infected endothelial cells could provide a source of continued virus replication in immune-compromised individuals, a context in which gammaherpesvirus-associated pathology frequently occurs.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plospath</journal-id>
<journal-title-group><journal-title>PLoS Pathogens</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7366</issn>
<issn pub-type="epub">1553-7374</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">18787698</article-id>
<article-id pub-id-type="pmc">2526176</article-id>
<article-id pub-id-type="publisher-id">07-PLPA-RA-0874R4</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1000152</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline"><subject>Microbiology</subject>
<subject>Microbiology</subject>
<subject>Virology</subject>
<subject>Virology</subject>
<subject>Virology/Animal Models of Infection</subject>
<subject>Virology/Animal Models of Infection</subject>
<subject>Virology/Host Invasion and Cell Entry</subject>
<subject>Virology/Host Invasion and Cell Entry</subject>
<subject>Virology/Immunodeficiency Viruses</subject>
<subject>Virology/Immunodeficiency Viruses</subject>
<subject>Virology/Persistence and Latency</subject>
<subject>Virology/Persistence and Latency</subject>
</subj-group>
</article-categories>
<title-group><article-title>Endothelial Cells Support Persistent Gammaherpesvirus 68 Infection</article-title>
<alt-title alt-title-type="running-head">Gammaherpesvirus Infection of Endothelial Cells</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Suárez</surname>
<given-names>Andrea Luísa</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>van Dyk</surname>
<given-names>Linda Faye</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Department of Microbiology and Program in Molecular Biology, University of Colorado Denver School of Medicine, Aurora, Colorado, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Department of Immunology, University of Colorado Denver School of Medicine, Aurora, Colorado, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Jung</surname>
<given-names>Jae U.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">University of Southern California School of Medicine, United States of America</aff>
<author-notes><corresp id="cor1">* E-mail: <email>Linda.VanDyk@uchsc.edu</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: ALS LFvD. Performed the experiments: ALS. Analyzed the data: ALS LFvD. Contributed reagents/materials/analysis tools: ALS LFvD. Wrote the paper: ALS LFvD.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>9</month>
<year>2008</year>
</pub-date>
<pub-date pub-type="epub"><day>12</day>
<month>9</month>
<year>2008</year>
</pub-date>
<volume>4</volume>
<issue>9</issue>
<elocation-id>e1000152</elocation-id>
<history><date date-type="received"><day>3</day>
<month>12</month>
<year>2007</year>
</date>
<date date-type="accepted"><day>12</day>
<month>8</month>
<year>2008</year>
</date>
</history>
<permissions><copyright-statement>Suárez, van Dyk.</copyright-statement>
<copyright-year>2008</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>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.</license-p>
</license>
</permissions>
<abstract><p>A variety of human diseases are associated with gammaherpesviruses, including neoplasms of lymphocytes (e.g. Burkitt's lymphoma) and endothelial cells (e.g. Kaposi's sarcoma). Gammaherpesvirus infections usually result in either a productive lytic infection, characterized by expression of all viral genes and rapid cell lysis, or latent infection, characterized by limited viral gene expression and no cell lysis. Here, we report characterization of endothelial cell infection with murine gammaherpesvirus 68 (γHV68), a virus phylogenetically related and biologically similar to the human gammaherpesviruses. Endothelial cells supported γHV68 replication <italic>in vitro</italic>
, but were unique in that a significant proportion of the cells escaped lysis, proliferated, and remained viable in culture for an extended time. Upon infection, endothelial cells became non-adherent and altered in size, complexity, and cell-surface protein expression. These cells were uniformly infected and expressed the lytic transcription program based on detection of abundant viral gene transcripts, GFP fluorescence from the viral genome, and viral surface protein expression. Additionally, endothelial cells continued to produce new infectious virions as late as 30 days post-infection. The outcome of this long-term infection was promoted by the γHV68 v-cyclin, because in the absence of the v-cyclin, viability was significantly reduced following infection. Importantly, infected primary endothelial cells also demonstrated increased viability relative to infected primary fibroblasts, and this increased viability was dependent on the v-cyclin. Finally, we provide evidence for infection of endothelial cells <italic>in vivo</italic>
in immune-deficient mice. The extended viability and virus production of infected endothelial cells indicated that endothelial cells provided a source of prolonged virus production and identify a cell-type specific adaptation of gammaherpesvirus replication. While infected endothelial cells would likely be cleared in a healthy individual, persistently infected endothelial cells could provide a source of continued virus replication in immune-compromised individuals, a context in which gammaherpesvirus-associated pathology frequently occurs.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>Various human diseases are associated with gammaherpesvirus infections, including neoplasms of lymphocytes (e.g. Burkitt's lymphoma) and endothelial cells (e.g. Kaposi's sarcoma). Gammaherpesvirus infection of cells usually results in either productive infection that is characterized by new virus production and rapid destruction of the host cell, or latent infection that is characterized by long-term carriage of viral DNA in intact cells that do not produce virus. Here, we characterize endothelial cell infection using a small animal model of gammaherpesvirus infection and disease. While infection of endothelial cells resulted in virus production as most cells do, infection of this cell type was unique in that cells remained intact and continued to proliferate. These intact, infected endothelial cells were significantly altered in appearance and gene expression compared to uninfected cells, changes predicted to impact endothelial cell growth and function. Endothelial cells were unique in their ability to support this type of persistent infection. These data demonstrate an additional mechanism, beyond latency, by which gammaherpesviruses may achieve long-term propagation, particularly in conditions of immune suppression. Our results suggest persistently infected cells as a therapeutic target for prevention/treatment of chronic disease, and may provide a mouse model for future testing.</p>
</abstract>
<counts><page-count count="16"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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