Identification of Quinolinones as Antivirals against Venezuelan Equine Encephalitis Virus
Venezuelan equine encephalitis virus (VEEV) is a reemerging alphavirus that can cause encephalitis resulting in severe human morbidity and mortality. Using a high-throughput cell-based screen, we identified a quinolinone compound that protected against VEEV-induced cytopathic effects. Analysis of vi...
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creator | Haese, Nicole N May, Nicholas A Taft-Benz, Sharon Moukha-Chafiq, Omar Madadi, Nikhil Zhang, Sixue Karyakarte, Shuklendu D Rodzinak, Kevin J Nguyen, Theresa H Denton, Michael Streblow, Aaron D Towers, Nichole A Rasmussen, Lynn Bostwick, Robert J Maddry, Joseph A Ananthan, Subramaniam Augelli-Szafran, Corinne E Suto, Mark J Sanders, Wes Moorman, Nathaniel DeFilippis, Victor Heise, Mark T Pathak, Ashish K Streblow, Daniel N Morrison, Thomas E |
description | Venezuelan equine encephalitis virus (VEEV) is a reemerging alphavirus that can cause encephalitis resulting in severe human morbidity and mortality. Using a high-throughput cell-based screen, we identified a quinolinone compound that protected against VEEV-induced cytopathic effects. Analysis of viral replication in cells identified several quinolinone compounds with potent inhibitory activity against vaccine and virulent strains of VEEV. These quinolinones also displayed inhibitory activity against additional alphaviruses, such as Mayaro virus and Ross River virus, although the potency was greatly reduced. Time-of-addition studies indicated that these compounds inhibit the early-to-mid stage of viral replication. Deep sequencing and reverse genetics studies identified two unique resistance mutations in the nsP2 gene (Y102S/C; stalk domain) that conferred VEEV resistance on this chemical series. Moreover, introduction of a K102Y mutation into the nsP2 gene enhanced the sensitivity of chikungunya virus (CHIKV) to this chemical series. Computational modeling of CHIKV and VEEV nsP2 identified a highly probable docking alignment for the quinolinone compounds that require a tyrosine residue at position 102 within the helicase stalk domain. These studies identified a class of compounds with antiviral activity against VEEV and other alphaviruses and provide further evidence that therapeutics targeting nsP2 may be useful against alphavirus infection. |
doi_str_mv | 10.1128/AAC.00244-21 |
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Using a high-throughput cell-based screen, we identified a quinolinone compound that protected against VEEV-induced cytopathic effects. Analysis of viral replication in cells identified several quinolinone compounds with potent inhibitory activity against vaccine and virulent strains of VEEV. These quinolinones also displayed inhibitory activity against additional alphaviruses, such as Mayaro virus and Ross River virus, although the potency was greatly reduced. Time-of-addition studies indicated that these compounds inhibit the early-to-mid stage of viral replication. Deep sequencing and reverse genetics studies identified two unique resistance mutations in the nsP2 gene (Y102S/C; stalk domain) that conferred VEEV resistance on this chemical series. Moreover, introduction of a K102Y mutation into the nsP2 gene enhanced the sensitivity of chikungunya virus (CHIKV) to this chemical series. Computational modeling of CHIKV and VEEV nsP2 identified a highly probable docking alignment for the quinolinone compounds that require a tyrosine residue at position 102 within the helicase stalk domain. These studies identified a class of compounds with antiviral activity against VEEV and other alphaviruses and provide further evidence that therapeutics targeting nsP2 may be useful against alphavirus infection.</description><identifier>ISSN: 0066-4804</identifier><identifier>EISSN: 1098-6596</identifier><identifier>DOI: 10.1128/AAC.00244-21</identifier><identifier>PMID: 34152810</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Animals ; Antiviral Agents ; Antiviral Agents - pharmacology ; Chikungunya virus ; Encephalitis Virus, Venezuelan Equine - genetics ; Horses ; Humans ; Quinolones - pharmacology ; Virus Replication</subject><ispartof>Antimicrobial agents and chemotherapy, 2021-08, Vol.65 (9), p.e0024421-e0024421</ispartof><rights>Copyright © 2021 American Society for Microbiology.</rights><rights>Copyright © 2021 American Society for Microbiology. 2021 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a418t-f6df8a8bb74461f1a6b57c7166f988ffe04eae81f8942f6fa6ffe7fda316dcd03</citedby><cites>FETCH-LOGICAL-a418t-f6df8a8bb74461f1a6b57c7166f988ffe04eae81f8942f6fa6ffe7fda316dcd03</cites><orcidid>0000-0002-1811-2938 ; 0000-0001-5829-8477</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8373297/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8373297/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34152810$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Haese, Nicole N</creatorcontrib><creatorcontrib>May, Nicholas A</creatorcontrib><creatorcontrib>Taft-Benz, Sharon</creatorcontrib><creatorcontrib>Moukha-Chafiq, Omar</creatorcontrib><creatorcontrib>Madadi, Nikhil</creatorcontrib><creatorcontrib>Zhang, Sixue</creatorcontrib><creatorcontrib>Karyakarte, Shuklendu D</creatorcontrib><creatorcontrib>Rodzinak, Kevin J</creatorcontrib><creatorcontrib>Nguyen, Theresa H</creatorcontrib><creatorcontrib>Denton, Michael</creatorcontrib><creatorcontrib>Streblow, Aaron D</creatorcontrib><creatorcontrib>Towers, Nichole A</creatorcontrib><creatorcontrib>Rasmussen, Lynn</creatorcontrib><creatorcontrib>Bostwick, Robert J</creatorcontrib><creatorcontrib>Maddry, Joseph A</creatorcontrib><creatorcontrib>Ananthan, Subramaniam</creatorcontrib><creatorcontrib>Augelli-Szafran, Corinne E</creatorcontrib><creatorcontrib>Suto, Mark J</creatorcontrib><creatorcontrib>Sanders, Wes</creatorcontrib><creatorcontrib>Moorman, Nathaniel</creatorcontrib><creatorcontrib>DeFilippis, Victor</creatorcontrib><creatorcontrib>Heise, Mark T</creatorcontrib><creatorcontrib>Pathak, Ashish K</creatorcontrib><creatorcontrib>Streblow, Daniel N</creatorcontrib><creatorcontrib>Morrison, Thomas E</creatorcontrib><title>Identification of Quinolinones as Antivirals against Venezuelan Equine Encephalitis Virus</title><title>Antimicrobial agents and chemotherapy</title><addtitle>Antimicrob Agents Chemother</addtitle><addtitle>Antimicrob Agents Chemother</addtitle><description>Venezuelan equine encephalitis virus (VEEV) is a reemerging alphavirus that can cause encephalitis resulting in severe human morbidity and mortality. Using a high-throughput cell-based screen, we identified a quinolinone compound that protected against VEEV-induced cytopathic effects. Analysis of viral replication in cells identified several quinolinone compounds with potent inhibitory activity against vaccine and virulent strains of VEEV. These quinolinones also displayed inhibitory activity against additional alphaviruses, such as Mayaro virus and Ross River virus, although the potency was greatly reduced. Time-of-addition studies indicated that these compounds inhibit the early-to-mid stage of viral replication. Deep sequencing and reverse genetics studies identified two unique resistance mutations in the nsP2 gene (Y102S/C; stalk domain) that conferred VEEV resistance on this chemical series. Moreover, introduction of a K102Y mutation into the nsP2 gene enhanced the sensitivity of chikungunya virus (CHIKV) to this chemical series. Computational modeling of CHIKV and VEEV nsP2 identified a highly probable docking alignment for the quinolinone compounds that require a tyrosine residue at position 102 within the helicase stalk domain. These studies identified a class of compounds with antiviral activity against VEEV and other alphaviruses and provide further evidence that therapeutics targeting nsP2 may be useful against alphavirus infection.</description><subject>Animals</subject><subject>Antiviral Agents</subject><subject>Antiviral Agents - pharmacology</subject><subject>Chikungunya virus</subject><subject>Encephalitis Virus, Venezuelan Equine - genetics</subject><subject>Horses</subject><subject>Humans</subject><subject>Quinolones - pharmacology</subject><subject>Virus Replication</subject><issn>0066-4804</issn><issn>1098-6596</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kd1LwzAUxYMobn68-Sx9VLAzN03T9EUoY37AQAQVfApZm2wZXbI17UD_eqObQx98COHm_nJuTg5CZ4AHAIRfF8VwgDGhNCawh_qAcx6zNGf7qI8xYzHlmPbQkfdzHOo0x4eol1BICQfcR28PlbKt0aaUrXE2cjp66ox1dVhW-Uj6qAj9tWlkHaqpNNa30auy6qNTtbTRaBVwFY1sqZYzWZvW-OjVNJ0_QQc63FGn2_0YvdyOnof38fjx7mFYjGNJgbexZpXmkk8mGaUMNEg2SbMyA8Z0zrnWClMlFQfNc0o005KFs0xXMgFWlRVOjtHNRnfZTRaqKoOd8FaxbMxCNu_CSSP-dqyZialbC55kCcmzIHCxFWjcqlO-FQvjS1UHd8p1XpCUUsgAMwjo1QYtG-d9o_RuDGDxlYYIaYjvNAT5wi83uPQLIuaua2z4if_Y8982dsI_USWfP42Uug</recordid><startdate>20210817</startdate><enddate>20210817</enddate><creator>Haese, Nicole N</creator><creator>May, Nicholas A</creator><creator>Taft-Benz, Sharon</creator><creator>Moukha-Chafiq, Omar</creator><creator>Madadi, Nikhil</creator><creator>Zhang, Sixue</creator><creator>Karyakarte, Shuklendu D</creator><creator>Rodzinak, Kevin J</creator><creator>Nguyen, Theresa H</creator><creator>Denton, Michael</creator><creator>Streblow, Aaron D</creator><creator>Towers, Nichole A</creator><creator>Rasmussen, Lynn</creator><creator>Bostwick, Robert J</creator><creator>Maddry, Joseph A</creator><creator>Ananthan, Subramaniam</creator><creator>Augelli-Szafran, Corinne E</creator><creator>Suto, Mark J</creator><creator>Sanders, Wes</creator><creator>Moorman, Nathaniel</creator><creator>DeFilippis, Victor</creator><creator>Heise, Mark T</creator><creator>Pathak, Ashish K</creator><creator>Streblow, Daniel N</creator><creator>Morrison, Thomas E</creator><general>American Society for Microbiology</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>5PM</scope><orcidid>https://orcid.org/0000-0002-1811-2938</orcidid><orcidid>https://orcid.org/0000-0001-5829-8477</orcidid></search><sort><creationdate>20210817</creationdate><title>Identification of Quinolinones as Antivirals against Venezuelan Equine Encephalitis Virus</title><author>Haese, Nicole N ; May, Nicholas A ; Taft-Benz, Sharon ; Moukha-Chafiq, Omar ; Madadi, Nikhil ; Zhang, Sixue ; Karyakarte, Shuklendu D ; Rodzinak, Kevin J ; Nguyen, Theresa H ; Denton, Michael ; Streblow, Aaron D ; Towers, Nichole A ; Rasmussen, Lynn ; Bostwick, Robert J ; Maddry, Joseph A ; Ananthan, Subramaniam ; Augelli-Szafran, Corinne E ; Suto, Mark J ; Sanders, Wes ; Moorman, Nathaniel ; DeFilippis, Victor ; Heise, Mark T ; Pathak, Ashish K ; Streblow, Daniel N ; Morrison, Thomas E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a418t-f6df8a8bb74461f1a6b57c7166f988ffe04eae81f8942f6fa6ffe7fda316dcd03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Antiviral Agents</topic><topic>Antiviral Agents - pharmacology</topic><topic>Chikungunya virus</topic><topic>Encephalitis Virus, Venezuelan Equine - genetics</topic><topic>Horses</topic><topic>Humans</topic><topic>Quinolones - pharmacology</topic><topic>Virus Replication</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Haese, Nicole N</creatorcontrib><creatorcontrib>May, Nicholas A</creatorcontrib><creatorcontrib>Taft-Benz, Sharon</creatorcontrib><creatorcontrib>Moukha-Chafiq, Omar</creatorcontrib><creatorcontrib>Madadi, Nikhil</creatorcontrib><creatorcontrib>Zhang, Sixue</creatorcontrib><creatorcontrib>Karyakarte, Shuklendu D</creatorcontrib><creatorcontrib>Rodzinak, Kevin J</creatorcontrib><creatorcontrib>Nguyen, Theresa H</creatorcontrib><creatorcontrib>Denton, Michael</creatorcontrib><creatorcontrib>Streblow, Aaron D</creatorcontrib><creatorcontrib>Towers, Nichole A</creatorcontrib><creatorcontrib>Rasmussen, Lynn</creatorcontrib><creatorcontrib>Bostwick, Robert J</creatorcontrib><creatorcontrib>Maddry, Joseph A</creatorcontrib><creatorcontrib>Ananthan, Subramaniam</creatorcontrib><creatorcontrib>Augelli-Szafran, Corinne E</creatorcontrib><creatorcontrib>Suto, Mark J</creatorcontrib><creatorcontrib>Sanders, Wes</creatorcontrib><creatorcontrib>Moorman, Nathaniel</creatorcontrib><creatorcontrib>DeFilippis, Victor</creatorcontrib><creatorcontrib>Heise, Mark T</creatorcontrib><creatorcontrib>Pathak, Ashish K</creatorcontrib><creatorcontrib>Streblow, Daniel N</creatorcontrib><creatorcontrib>Morrison, Thomas E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Antimicrobial agents and chemotherapy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Haese, Nicole N</au><au>May, Nicholas A</au><au>Taft-Benz, Sharon</au><au>Moukha-Chafiq, Omar</au><au>Madadi, Nikhil</au><au>Zhang, Sixue</au><au>Karyakarte, Shuklendu D</au><au>Rodzinak, Kevin J</au><au>Nguyen, Theresa H</au><au>Denton, Michael</au><au>Streblow, Aaron D</au><au>Towers, Nichole A</au><au>Rasmussen, Lynn</au><au>Bostwick, Robert J</au><au>Maddry, Joseph A</au><au>Ananthan, Subramaniam</au><au>Augelli-Szafran, Corinne E</au><au>Suto, Mark J</au><au>Sanders, Wes</au><au>Moorman, Nathaniel</au><au>DeFilippis, Victor</au><au>Heise, Mark T</au><au>Pathak, Ashish K</au><au>Streblow, Daniel N</au><au>Morrison, Thomas E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of Quinolinones as Antivirals against Venezuelan Equine Encephalitis Virus</atitle><jtitle>Antimicrobial agents and chemotherapy</jtitle><stitle>Antimicrob Agents Chemother</stitle><addtitle>Antimicrob Agents Chemother</addtitle><date>2021-08-17</date><risdate>2021</risdate><volume>65</volume><issue>9</issue><spage>e0024421</spage><epage>e0024421</epage><pages>e0024421-e0024421</pages><issn>0066-4804</issn><eissn>1098-6596</eissn><abstract>Venezuelan equine encephalitis virus (VEEV) is a reemerging alphavirus that can cause encephalitis resulting in severe human morbidity and mortality. Using a high-throughput cell-based screen, we identified a quinolinone compound that protected against VEEV-induced cytopathic effects. Analysis of viral replication in cells identified several quinolinone compounds with potent inhibitory activity against vaccine and virulent strains of VEEV. These quinolinones also displayed inhibitory activity against additional alphaviruses, such as Mayaro virus and Ross River virus, although the potency was greatly reduced. Time-of-addition studies indicated that these compounds inhibit the early-to-mid stage of viral replication. Deep sequencing and reverse genetics studies identified two unique resistance mutations in the nsP2 gene (Y102S/C; stalk domain) that conferred VEEV resistance on this chemical series. Moreover, introduction of a K102Y mutation into the nsP2 gene enhanced the sensitivity of chikungunya virus (CHIKV) to this chemical series. Computational modeling of CHIKV and VEEV nsP2 identified a highly probable docking alignment for the quinolinone compounds that require a tyrosine residue at position 102 within the helicase stalk domain. These studies identified a class of compounds with antiviral activity against VEEV and other alphaviruses and provide further evidence that therapeutics targeting nsP2 may be useful against alphavirus infection.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>34152810</pmid><doi>10.1128/AAC.00244-21</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-1811-2938</orcidid><orcidid>https://orcid.org/0000-0001-5829-8477</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antiviral Agents Antiviral Agents - pharmacology Chikungunya virus Encephalitis Virus, Venezuelan Equine - genetics Horses Humans Quinolones - pharmacology Virus Replication |
title | Identification of Quinolinones as Antivirals against Venezuelan Equine Encephalitis Virus |
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