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Differences in type I interferon signaling antagonism by dengue viruses in human and non-human primate cell lines
In vitro studies have shown that dengue virus (DENV) can thwart the actions of interferon (IFN)-α/β and prevent the development of an antiviral state in infected cells. Clinical studies looking at gene expression in patients with severe dengue show a reduced expression of interferon stimulated genes...
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| Published in: | PLoS neglected tropical diseases 2015-03, Vol.9 (3), p.e0003468-e0003468 |
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| description | In vitro studies have shown that dengue virus (DENV) can thwart the actions of interferon (IFN)-α/β and prevent the development of an antiviral state in infected cells. Clinical studies looking at gene expression in patients with severe dengue show a reduced expression of interferon stimulated genes compared to patients with dengue fever. Interestingly, there are conflicting reports as to the ability of DENV or other flaviviruses to inhibit IFN-α/β signaling.
In order to determine the relative inhibition of IFN-α/β signaling by DENVs, a method combining flow cytometry and a four-parameter logistic regression model was established. A representative isolate from DENV-1, -3 and -4 and seventeen representative isolates encompassing all DENV-2 genotypes were evaluated. All of the DENVs evaluated in this study were capable of inhibiting IFN-α/β signaling. Most of the strains were able to inhibit IFN-α/β to a degree similar to DENV strain 16681; however, DENV-2 sylvatic strains demonstrated an increased inhibition of phosphorylated signal transducer and activator of transcription (pSTAT1). Surprisingly, we were unable to observe inhibition of pSTAT1 by DENV-2 sylvatic strains or the Asian strain 16681 in non-human primate (NHP) cell lines. Analysis in primary Rhesus macaque dendritic cells suggests that DENVs are capable of inhibiting IFN signaling in these cells. However, contrary to human dendritic cells, production of IFN-α was detected in the supernatant of DENV-infected Rhesus macaque dendritic cells.
The ability of DENVs to inhibit IFN-α/β signaling is conserved. Although some variation in the inhibition was observed, the moderate differences may be difficult to correlate with clinical outcomes. DENVs were unable to inhibit pSTAT1 in NHP cell lines, but their ability to inhibit pSTAT1 in primary Rhesus macaque dendritic cells suggests that this may be a cell specific phenomena or due to the transformed nature of the cell lines. |
| doi_str_mv | 10.1371/journal.pntd.0003468 |
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In order to determine the relative inhibition of IFN-α/β signaling by DENVs, a method combining flow cytometry and a four-parameter logistic regression model was established. A representative isolate from DENV-1, -3 and -4 and seventeen representative isolates encompassing all DENV-2 genotypes were evaluated. All of the DENVs evaluated in this study were capable of inhibiting IFN-α/β signaling. Most of the strains were able to inhibit IFN-α/β to a degree similar to DENV strain 16681; however, DENV-2 sylvatic strains demonstrated an increased inhibition of phosphorylated signal transducer and activator of transcription (pSTAT1). Surprisingly, we were unable to observe inhibition of pSTAT1 by DENV-2 sylvatic strains or the Asian strain 16681 in non-human primate (NHP) cell lines. Analysis in primary Rhesus macaque dendritic cells suggests that DENVs are capable of inhibiting IFN signaling in these cells. However, contrary to human dendritic cells, production of IFN-α was detected in the supernatant of DENV-infected Rhesus macaque dendritic cells.
The ability of DENVs to inhibit IFN-α/β signaling is conserved. Although some variation in the inhibition was observed, the moderate differences may be difficult to correlate with clinical outcomes. DENVs were unable to inhibit pSTAT1 in NHP cell lines, but their ability to inhibit pSTAT1 in primary Rhesus macaque dendritic cells suggests that this may be a cell specific phenomena or due to the transformed nature of the cell lines.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0003468</identifier><identifier>PMID: 25768016</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Binding sites ; Cell Line ; Clinical outcomes ; Comparative analysis ; Dendritic cells ; Dendritic Cells - metabolism ; Dengue ; Dengue fever ; Dengue virus ; Dengue Virus - physiology ; Dengue viruses ; Development and progression ; Experiments ; Gene expression ; Genomes ; Humans ; Illnesses ; Infections ; Interferon ; Interferon Type I - physiology ; Macaca mulatta ; Phosphorylation ; Phylogenetics ; Physiological aspects ; Proteins ; Signal Transduction - physiology ; STAT1 Transcription Factor - metabolism ; STAT2 Transcription Factor - metabolism ; Studies ; Tropical diseases ; Viral infections ; Virus Replication ; Viruses</subject><ispartof>PLoS neglected tropical diseases, 2015-03, Vol.9 (3), p.e0003468-e0003468</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>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: Medina FA, Torres-Malavé G, Chase AJ, Santiago GA, Medina JF, Santiago LM, et al. (2015) Differences in Type I Interferon Signaling Antagonism by Dengue Viruses in Human and Non-Human Primate Cell Lines. PLoS Negl Trop Dis 9(3): e0003468. doi:10.1371/journal.pntd.0003468</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c629t-125865a432177648ca6d5d8a73ff20efad205a6ec2bc22ff40098b995bbdf2903</citedby><cites>FETCH-LOGICAL-c629t-125865a432177648ca6d5d8a73ff20efad205a6ec2bc22ff40098b995bbdf2903</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4359095/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4359095/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,37048,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25768016$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>de Silva, Aravinda M</contributor><creatorcontrib>Medina, Freddy A</creatorcontrib><creatorcontrib>Torres-Malavé, Giselle</creatorcontrib><creatorcontrib>Chase, Amanda J</creatorcontrib><creatorcontrib>Santiago, Gilberto A</creatorcontrib><creatorcontrib>Medina, Juan F</creatorcontrib><creatorcontrib>Santiago, Luis M</creatorcontrib><creatorcontrib>Muñoz-Jordán, Jorge L</creatorcontrib><title>Differences in type I interferon signaling antagonism by dengue viruses in human and non-human primate cell lines</title><title>PLoS neglected tropical diseases</title><addtitle>PLoS Negl Trop Dis</addtitle><description>In vitro studies have shown that dengue virus (DENV) can thwart the actions of interferon (IFN)-α/β and prevent the development of an antiviral state in infected cells. Clinical studies looking at gene expression in patients with severe dengue show a reduced expression of interferon stimulated genes compared to patients with dengue fever. Interestingly, there are conflicting reports as to the ability of DENV or other flaviviruses to inhibit IFN-α/β signaling.
In order to determine the relative inhibition of IFN-α/β signaling by DENVs, a method combining flow cytometry and a four-parameter logistic regression model was established. A representative isolate from DENV-1, -3 and -4 and seventeen representative isolates encompassing all DENV-2 genotypes were evaluated. All of the DENVs evaluated in this study were capable of inhibiting IFN-α/β signaling. Most of the strains were able to inhibit IFN-α/β to a degree similar to DENV strain 16681; however, DENV-2 sylvatic strains demonstrated an increased inhibition of phosphorylated signal transducer and activator of transcription (pSTAT1). Surprisingly, we were unable to observe inhibition of pSTAT1 by DENV-2 sylvatic strains or the Asian strain 16681 in non-human primate (NHP) cell lines. Analysis in primary Rhesus macaque dendritic cells suggests that DENVs are capable of inhibiting IFN signaling in these cells. However, contrary to human dendritic cells, production of IFN-α was detected in the supernatant of DENV-infected Rhesus macaque dendritic cells.
The ability of DENVs to inhibit IFN-α/β signaling is conserved. Although some variation in the inhibition was observed, the moderate differences may be difficult to correlate with clinical outcomes. DENVs were unable to inhibit pSTAT1 in NHP cell lines, but their ability to inhibit pSTAT1 in primary Rhesus macaque dendritic cells suggests that this may be a cell specific phenomena or due to the transformed nature of the cell lines.</description><subject>Animals</subject><subject>Binding sites</subject><subject>Cell Line</subject><subject>Clinical outcomes</subject><subject>Comparative analysis</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - metabolism</subject><subject>Dengue</subject><subject>Dengue fever</subject><subject>Dengue virus</subject><subject>Dengue Virus - physiology</subject><subject>Dengue viruses</subject><subject>Development and progression</subject><subject>Experiments</subject><subject>Gene expression</subject><subject>Genomes</subject><subject>Humans</subject><subject>Illnesses</subject><subject>Infections</subject><subject>Interferon</subject><subject>Interferon Type I - physiology</subject><subject>Macaca mulatta</subject><subject>Phosphorylation</subject><subject>Phylogenetics</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Signal Transduction - physiology</subject><subject>STAT1 Transcription Factor - metabolism</subject><subject>STAT2 Transcription Factor - metabolism</subject><subject>Studies</subject><subject>Tropical diseases</subject><subject>Viral infections</subject><subject>Virus Replication</subject><subject>Viruses</subject><issn>1935-2735</issn><issn>1935-2727</issn><issn>1935-2735</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqNkk2L2zAQhk1p6W63_QelNRRKL0n1belSWLZfgYVe2rOQ5ZGj4EhZyV7Iv6-yzi4J9FB8kDR-3ndGo6mqtxgtMW3w502cUjDDchfGbokQokzIZ9UlVpQvSEP585P9RfUq5w1CXHGJX1YXhDdCIiwuq7uv3jlIECzk2od63O-gXpXdCKnEY6iz70saH_rahNH0Mfi8rdt93UHoJ6jvfZryrF1PWxMK1dUhhsV82iW_NSPUFoahLi6QX1cvnBkyvDmuV9Wf799-3_xc3P76sbq5vl1YQdS4wIRLwQ2jBDeNYNIa0fFOmoY6RxA40xHEjQBLWkuIcwwhJVuleNt2jihEr6r3s-9uiFkfu5U1FgqjhgkqCrGaiS6ajX6oNO11NF4_BGLqtUmjtwNoJVQHzBHGmGHSNS00SCHEpLROCQ7F68sx29RuobMQxmSGM9PzP8GvdR_vNaNcIcWLwaejQYp3E-RRb30-dM0EiNOh7qbU3FBC_wMVjGCOyvNfVR9mtDflFj64WJLbA66vGZZKEiZIoZb_oMrXwdbbGMD5Ej8TfDwRrMEM4zrHYRp9DPkcZDNoU8w5gXvqCEb6MMaPD6MPY6yPY1xk7067-SR6nFv6F6TU77c</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Medina, Freddy A</creator><creator>Torres-Malavé, Giselle</creator><creator>Chase, Amanda J</creator><creator>Santiago, Gilberto A</creator><creator>Medina, Juan F</creator><creator>Santiago, Luis M</creator><creator>Muñoz-Jordán, Jorge L</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7T2</scope><scope>7U2</scope><scope>7U9</scope><scope>C1K</scope><scope>F1W</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150301</creationdate><title>Differences in type I interferon signaling antagonism by dengue viruses in human and non-human primate cell lines</title><author>Medina, Freddy A ; 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Performed the experiments: FAM GTM AJC GAS JFM. Analyzed the data: FAM GTM AJC GAS LMS JLM. Wrote the paper: FAM JLM.</notes><notes>The authors have declared that no competing interests exist.</notes><abstract>In vitro studies have shown that dengue virus (DENV) can thwart the actions of interferon (IFN)-α/β and prevent the development of an antiviral state in infected cells. Clinical studies looking at gene expression in patients with severe dengue show a reduced expression of interferon stimulated genes compared to patients with dengue fever. Interestingly, there are conflicting reports as to the ability of DENV or other flaviviruses to inhibit IFN-α/β signaling.
In order to determine the relative inhibition of IFN-α/β signaling by DENVs, a method combining flow cytometry and a four-parameter logistic regression model was established. A representative isolate from DENV-1, -3 and -4 and seventeen representative isolates encompassing all DENV-2 genotypes were evaluated. All of the DENVs evaluated in this study were capable of inhibiting IFN-α/β signaling. Most of the strains were able to inhibit IFN-α/β to a degree similar to DENV strain 16681; however, DENV-2 sylvatic strains demonstrated an increased inhibition of phosphorylated signal transducer and activator of transcription (pSTAT1). Surprisingly, we were unable to observe inhibition of pSTAT1 by DENV-2 sylvatic strains or the Asian strain 16681 in non-human primate (NHP) cell lines. Analysis in primary Rhesus macaque dendritic cells suggests that DENVs are capable of inhibiting IFN signaling in these cells. However, contrary to human dendritic cells, production of IFN-α was detected in the supernatant of DENV-infected Rhesus macaque dendritic cells.
The ability of DENVs to inhibit IFN-α/β signaling is conserved. Although some variation in the inhibition was observed, the moderate differences may be difficult to correlate with clinical outcomes. DENVs were unable to inhibit pSTAT1 in NHP cell lines, but their ability to inhibit pSTAT1 in primary Rhesus macaque dendritic cells suggests that this may be a cell specific phenomena or due to the transformed nature of the cell lines.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25768016</pmid><doi>10.1371/journal.pntd.0003468</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Binding sites Cell Line Clinical outcomes Comparative analysis Dendritic cells Dendritic Cells - metabolism Dengue Dengue fever Dengue virus Dengue Virus - physiology Dengue viruses Development and progression Experiments Gene expression Genomes Humans Illnesses Infections Interferon Interferon Type I - physiology Macaca mulatta Phosphorylation Phylogenetics Physiological aspects Proteins Signal Transduction - physiology STAT1 Transcription Factor - metabolism STAT2 Transcription Factor - metabolism Studies Tropical diseases Viral infections Virus Replication Viruses |
| title | Differences in type I interferon signaling antagonism by dengue viruses in human and non-human primate cell lines |
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