Determining the Mutation Bias of Favipiravir in Influenza Virus Using Next-Generation Sequencing.
Identifieur interne : 000205 ( PubMed/Corpus ); précédent : 000204; suivant : 000206Determining the Mutation Bias of Favipiravir in Influenza Virus Using Next-Generation Sequencing.
Auteurs : Daniel H. Goldhill ; Pinky Langat ; Hongyao Xie ; Monica Galiano ; Shahjahan Miah ; Paul Kellam ; Maria Zambon ; Angie Lackenby ; Wendy S. BarclaySource :
- Journal of virology [ 1098-5514 ] ; 2019.
English descriptors
- KwdEn :
- Amides (pharmacology), Animals, Bias, DNA Primers (genetics), Dogs, HEK293 Cells, High-Throughput Nucleotide Sequencing (methods), Humans, Influenza A virus (drug effects), Influenza A virus (genetics), Madin Darby Canine Kidney Cells, Mutation, Pyrazines (pharmacology), Sequence Analysis, RNA, Whole Genome Sequencing.
- MESH :
- chemical , genetics : DNA Primers.
- chemical , pharmacology : Amides, Pyrazines.
- drug effects : Influenza A virus.
- genetics : Influenza A virus.
- methods : High-Throughput Nucleotide Sequencing.
- Animals, Bias, Dogs, HEK293 Cells, Humans, Madin Darby Canine Kidney Cells, Mutation, Sequence Analysis, RNA, Whole Genome Sequencing.
Abstract
Favipiravir is a broad-spectrum antiviral drug that may be used to treat influenza. Previous research has identified that favipiravir likely acts as a mutagen, but the precise mutation bias that favipiravir induces in influenza virus RNAs has not been described. Here, we use next-generation sequencing (NGS) with barcoding of individual RNA molecules to accurately and quantitatively detect favipiravir-induced mutations and to sample orders of magnitude more mutations than would be possible through Sanger sequencing. We demonstrate that favipiravir causes mutations and show that favipiravir primarily acts as a guanine analogue and secondarily as an adenine analogue resulting in the accumulation of transition mutations. We also use a standard NGS pipeline to show that the mutagenic effect of favipiravir can be measured by whole-genome sequencing of virus.IMPORTANCE New antiviral drugs are needed as a first line of defense in the event of a novel influenza pandemic. Favipiravir is a broad-spectrum antiviral which is effective against influenza. The exact mechanism of how favipiravir works to inhibit influenza is still unclear. We used next-generation sequencing (NGS) to demonstrate that favipiravir causes mutations in influenza RNA. The greater depth of NGS sequence information over traditional sequencing methods allowed us to precisely determine the bias of particular mutations caused by favipiravir. NGS can also be used in a standard diagnostic pipeline to show that favipiravir is acting on the virus by revealing the mutation bias pattern typical to the drug. Our work will aid in testing whether viruses are resistant to favipiravir and may help demonstrate the effect of favipiravir on viruses in a clinical setting. This will be important if favipiravir is used during a future influenza pandemic.
DOI: 10.1128/JVI.01217-18
PubMed: 30381482
Links to Exploration step
pubmed:30381482Le document en format XML
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Goldhill</name><affiliation><nlm:affiliation>Public Health England, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Langat, Pinky" sort="Langat, Pinky" uniqKey="Langat P" first="Pinky" last="Langat">Pinky Langat</name><affiliation><nlm:affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Xie, Hongyao" sort="Xie, Hongyao" uniqKey="Xie H" first="Hongyao" last="Xie">Hongyao Xie</name><affiliation><nlm:affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Galiano, Monica" sort="Galiano, Monica" uniqKey="Galiano M" first="Monica" last="Galiano">Monica Galiano</name><affiliation><nlm:affiliation>Public Health England, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Miah, Shahjahan" sort="Miah, Shahjahan" uniqKey="Miah S" first="Shahjahan" last="Miah">Shahjahan Miah</name><affiliation><nlm:affiliation>Public Health England, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Kellam, Paul" sort="Kellam, Paul" uniqKey="Kellam P" first="Paul" last="Kellam">Paul Kellam</name><affiliation><nlm:affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Zambon, Maria" sort="Zambon, Maria" uniqKey="Zambon M" first="Maria" last="Zambon">Maria Zambon</name><affiliation><nlm:affiliation>Public Health England, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Lackenby, Angie" sort="Lackenby, Angie" uniqKey="Lackenby A" first="Angie" last="Lackenby">Angie Lackenby</name><affiliation><nlm:affiliation>Public Health England, London, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Barclay, Wendy S" sort="Barclay, Wendy S" uniqKey="Barclay W" first="Wendy S" last="Barclay">Wendy S. Barclay</name><affiliation><nlm:affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom w.barclay@imperial.ac.uk.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of virology</title><idno type="eISSN">1098-5514</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amides (pharmacology)</term><term>Animals</term><term>Bias</term><term>DNA Primers (genetics)</term><term>Dogs</term><term>HEK293 Cells</term><term>High-Throughput Nucleotide Sequencing (methods)</term><term>Humans</term><term>Influenza A virus (drug effects)</term><term>Influenza A virus (genetics)</term><term>Madin Darby Canine Kidney Cells</term><term>Mutation</term><term>Pyrazines (pharmacology)</term><term>Sequence Analysis, RNA</term><term>Whole Genome Sequencing</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>DNA Primers</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Amides</term><term>Pyrazines</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Influenza A virus</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Influenza A virus</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>High-Throughput Nucleotide Sequencing</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Bias</term><term>Dogs</term><term>HEK293 Cells</term><term>Humans</term><term>Madin Darby Canine Kidney Cells</term><term>Mutation</term><term>Sequence Analysis, RNA</term><term>Whole Genome Sequencing</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Favipiravir is a broad-spectrum antiviral drug that may be used to treat influenza. Previous research has identified that favipiravir likely acts as a mutagen, but the precise mutation bias that favipiravir induces in influenza virus RNAs has not been described. Here, we use next-generation sequencing (NGS) with barcoding of individual RNA molecules to accurately and quantitatively detect favipiravir-induced mutations and to sample orders of magnitude more mutations than would be possible through Sanger sequencing. We demonstrate that favipiravir causes mutations and show that favipiravir primarily acts as a guanine analogue and secondarily as an adenine analogue resulting in the accumulation of transition mutations. We also use a standard NGS pipeline to show that the mutagenic effect of favipiravir can be measured by whole-genome sequencing of virus.<b>IMPORTANCE</b> New antiviral drugs are needed as a first line of defense in the event of a novel influenza pandemic. Favipiravir is a broad-spectrum antiviral which is effective against influenza. The exact mechanism of how favipiravir works to inhibit influenza is still unclear. We used next-generation sequencing (NGS) to demonstrate that favipiravir causes mutations in influenza RNA. The greater depth of NGS sequence information over traditional sequencing methods allowed us to precisely determine the bias of particular mutations caused by favipiravir. NGS can also be used in a standard diagnostic pipeline to show that favipiravir is acting on the virus by revealing the mutation bias pattern typical to the drug. Our work will aid in testing whether viruses are resistant to favipiravir and may help demonstrate the effect of favipiravir on viruses in a clinical setting. This will be important if favipiravir is used during a future influenza pandemic.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30381482</PMID><DateCompleted><Year>2019</Year><Month>10</Month><Day>22</Day></DateCompleted><DateRevised><Year>2020</Year><Month>04</Month><Day>21</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">1098-5514</ISSN><JournalIssue CitedMedium="Internet"><Volume>93</Volume><Issue>2</Issue><PubDate><Year>2019</Year><Month>01</Month><Day>15</Day></PubDate></JournalIssue><Title>Journal of virology</Title><ISOAbbreviation>J. Virol.</ISOAbbreviation></Journal><ArticleTitle>Determining the Mutation Bias of Favipiravir in Influenza Virus Using Next-Generation Sequencing.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e01217-18</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.01217-18</ELocationID><Abstract><AbstractText>Favipiravir is a broad-spectrum antiviral drug that may be used to treat influenza. Previous research has identified that favipiravir likely acts as a mutagen, but the precise mutation bias that favipiravir induces in influenza virus RNAs has not been described. Here, we use next-generation sequencing (NGS) with barcoding of individual RNA molecules to accurately and quantitatively detect favipiravir-induced mutations and to sample orders of magnitude more mutations than would be possible through Sanger sequencing. We demonstrate that favipiravir causes mutations and show that favipiravir primarily acts as a guanine analogue and secondarily as an adenine analogue resulting in the accumulation of transition mutations. We also use a standard NGS pipeline to show that the mutagenic effect of favipiravir can be measured by whole-genome sequencing of virus.<b>IMPORTANCE</b> New antiviral drugs are needed as a first line of defense in the event of a novel influenza pandemic. Favipiravir is a broad-spectrum antiviral which is effective against influenza. The exact mechanism of how favipiravir works to inhibit influenza is still unclear. We used next-generation sequencing (NGS) to demonstrate that favipiravir causes mutations in influenza RNA. The greater depth of NGS sequence information over traditional sequencing methods allowed us to precisely determine the bias of particular mutations caused by favipiravir. NGS can also be used in a standard diagnostic pipeline to show that favipiravir is acting on the virus by revealing the mutation bias pattern typical to the drug. Our work will aid in testing whether viruses are resistant to favipiravir and may help demonstrate the effect of favipiravir on viruses in a clinical setting. This will be important if favipiravir is used during a future influenza pandemic.</AbstractText><CopyrightInformation>Copyright © 2019 Goldhill et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Goldhill</LastName><ForeName>Daniel H</ForeName><Initials>DH</Initials><Identifier Source="ORCID">0000-0003-4597-5963</Identifier><AffiliationInfo><Affiliation>Public Health England, London, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Langat</LastName><ForeName>Pinky</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xie</LastName><ForeName>Hongyao</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Galiano</LastName><ForeName>Monica</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Public Health England, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Miah</LastName><ForeName>Shahjahan</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Public Health England, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kellam</LastName><ForeName>Paul</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zambon</LastName><ForeName>Maria</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Public Health England, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lackenby</LastName><ForeName>Angie</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Public Health England, London, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barclay</LastName><ForeName>Wendy S</ForeName><Initials>WS</Initials><AffiliationInfo><Affiliation>Department of Virology, Faculty of Medicine, Imperial College, London, United Kingdom w.barclay@imperial.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Agency>Wellcome Trust</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>200187/Z/15/Z</GrantID><Acronym>WT_</Acronym><Agency>Wellcome Trust</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>01</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Virol</MedlineTA><NlmUniqueID>0113724</NlmUniqueID><ISSNLinking>0022-538X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000577">Amides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D017931">DNA Primers</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D011719">Pyrazines</NameOfSubstance></Chemical><Chemical><RegistryNumber>EW5GL2X7E0</RegistryNumber><NameOfSubstance UI="C462182">favipiravir</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000577" MajorTopicYN="N">Amides</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015982" MajorTopicYN="N">Bias</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017931" MajorTopicYN="N">DNA Primers</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004285" MajorTopicYN="N">Dogs</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057809" MajorTopicYN="N">HEK293 Cells</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059014" MajorTopicYN="N">High-Throughput Nucleotide Sequencing</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="Y">methods</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009980" MajorTopicYN="N">Influenza A virus</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D061985" MajorTopicYN="N">Madin Darby Canine Kidney Cells</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009154" MajorTopicYN="Y">Mutation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011719" MajorTopicYN="N">Pyrazines</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017423" MajorTopicYN="N">Sequence Analysis, RNA</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000073336" MajorTopicYN="N">Whole Genome Sequencing</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Primer ID</Keyword><Keyword MajorTopicYN="Y">favipiravir</Keyword><Keyword MajorTopicYN="Y">influenza</Keyword><Keyword MajorTopicYN="Y">mutation bias</Keyword><Keyword MajorTopicYN="Y">next-generation sequencing</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>07</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>10</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>11</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>10</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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