Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse
Adaptive evolution is characterized by positive and parallel, or repeated selection of mutations. Mouse adaptation of influenza A virus (IAV) produces virulent mutants that demonstrate positive and parallel evolution of mutations in the hemagglutinin (HA) receptor and non-structural protein 1 (NS1)...
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| Veröffentlicht in: | PloS one 2011-06, Vol.6 (6), p.e21740-e21740 |
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| creator | Ping, Jihui Keleta, Liya Forbes, Nicole E Dankar, Samar Stecho, William Tyler, Shaun Zhou, Yan Babiuk, Lorne Weingartl, Hana Halpin, Rebecca A Boyne, Alex Bera, Jayati Hostetler, Jessicah Fedorova, Nadia B Proudfoot, Katie Katzel, Dan A Stockwell, Tim B Ghedin, Elodie Spiro, David J Brown, Earl G |
| description | Adaptive evolution is characterized by positive and parallel, or repeated selection of mutations. Mouse adaptation of influenza A virus (IAV) produces virulent mutants that demonstrate positive and parallel evolution of mutations in the hemagglutinin (HA) receptor and non-structural protein 1 (NS1) interferon antagonist genes. We now present a genomic analysis of all 11 genes of 39 mouse adapted IAV variants from 10 replicate adaptation experiments. Mutations were mapped on the primary and structural maps of each protein and specific mutations were validated with respect to virulence, replication, and RNA polymerase activity. Mouse adapted (MA) variants obtained after 12 or 20-21 serial infections acquired on average 5.8 and 7.9 nonsynonymous mutations per genome of 11 genes, respectively. Among a total of 115 nonsynonymous mutations, 51 demonstrated properties of natural selection including 27 parallel mutations. The greatest degree of parallel evolution occurred in the HA receptor and ribonucleocapsid components, polymerase subunits (PB1, PB2, PA) and NP. Mutations occurred in host nuclear trafficking factor binding sites as well as sites of virus-virus protein subunit interaction for NP, NS1, HA and NA proteins. Adaptive regions included cap binding and endonuclease domains in the PB2 and PA polymerase subunits. Four mutations in NS1 resulted in loss of binding to the host cleavage and polyadenylation specificity factor (CPSF30) suggesting that a reduction in inhibition of host gene expression was being selected. The most prevalent mutations in PB2 and NP were shown to increase virulence but differed in their ability to enhance replication and demonstrated epistatic effects. Several positively selected RNA polymerase mutations demonstrated increased virulence associated with >300% enhanced polymerase activity. Adaptive mutations that control host range and virulence were identified by their repeated selection to comprise a defined model for studying IAV evolution to increased virulence in the mouse. |
| doi_str_mv | 10.1371/journal.pone.0021740 |
| format | Article |
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Mouse adaptation of influenza A virus (IAV) produces virulent mutants that demonstrate positive and parallel evolution of mutations in the hemagglutinin (HA) receptor and non-structural protein 1 (NS1) interferon antagonist genes. We now present a genomic analysis of all 11 genes of 39 mouse adapted IAV variants from 10 replicate adaptation experiments. Mutations were mapped on the primary and structural maps of each protein and specific mutations were validated with respect to virulence, replication, and RNA polymerase activity. Mouse adapted (MA) variants obtained after 12 or 20-21 serial infections acquired on average 5.8 and 7.9 nonsynonymous mutations per genome of 11 genes, respectively. Among a total of 115 nonsynonymous mutations, 51 demonstrated properties of natural selection including 27 parallel mutations. The greatest degree of parallel evolution occurred in the HA receptor and ribonucleocapsid components, polymerase subunits (PB1, PB2, PA) and NP. Mutations occurred in host nuclear trafficking factor binding sites as well as sites of virus-virus protein subunit interaction for NP, NS1, HA and NA proteins. Adaptive regions included cap binding and endonuclease domains in the PB2 and PA polymerase subunits. Four mutations in NS1 resulted in loss of binding to the host cleavage and polyadenylation specificity factor (CPSF30) suggesting that a reduction in inhibition of host gene expression was being selected. The most prevalent mutations in PB2 and NP were shown to increase virulence but differed in their ability to enhance replication and demonstrated epistatic effects. Several positively selected RNA polymerase mutations demonstrated increased virulence associated with >300% enhanced polymerase activity. Adaptive mutations that control host range and virulence were identified by their repeated selection to comprise a defined model for studying IAV evolution to increased virulence in the mouse.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0021740</identifier><identifier>PMID: 21738783</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Adaptive control ; Analysis ; Animal experimentation ; Animals ; Binding sites ; Biochemistry ; Biological response modifiers ; Biology ; Cell Line ; DNA-directed RNA polymerase ; Dogs ; Drug resistance ; Endonuclease ; Epistasis ; Evolution ; Evolution & development ; Evolutionary biology ; Gene expression ; Gene mapping ; Genes ; Genetic research ; Genome, Viral - genetics ; Genomes ; Genomic analysis ; Genomics ; Health aspects ; Hemagglutinins ; Hepatitis ; Host range ; Human evolution ; Humans ; Immunology ; Infections ; Infectious diseases ; Influenza ; Influenza A ; Influenza A virus - genetics ; Influenza A virus - metabolism ; Interferon ; Medical research ; Medicine ; Mice ; Molecular biology ; Mutants ; Mutation ; Natural selection ; Pathogenesis ; Polyadenylation ; Protein binding ; Proteins ; Replication ; Ribonucleic acid ; RNA ; RNA polymerase ; Viral Proteins - genetics ; Viral Proteins - metabolism ; Virology ; Virulence ; Virulence (Microbiology) ; Virulence - genetics ; Virus replication ; Viruses</subject><ispartof>PloS one, 2011-06, Vol.6 (6), p.e21740-e21740</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-761ad73391426a3f06330bc1f14a5d6d57b3709910c5b17dd658b4aa792be6823</citedby><cites>FETCH-LOGICAL-c757t-761ad73391426a3f06330bc1f14a5d6d57b3709910c5b17dd658b4aa792be6823</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/PMC3128085/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3128085/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21738783$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zhang, Luwen</contributor><creatorcontrib>Ping, Jihui</creatorcontrib><creatorcontrib>Keleta, Liya</creatorcontrib><creatorcontrib>Forbes, Nicole E</creatorcontrib><creatorcontrib>Dankar, Samar</creatorcontrib><creatorcontrib>Stecho, William</creatorcontrib><creatorcontrib>Tyler, Shaun</creatorcontrib><creatorcontrib>Zhou, Yan</creatorcontrib><creatorcontrib>Babiuk, Lorne</creatorcontrib><creatorcontrib>Weingartl, Hana</creatorcontrib><creatorcontrib>Halpin, Rebecca A</creatorcontrib><creatorcontrib>Boyne, Alex</creatorcontrib><creatorcontrib>Bera, Jayati</creatorcontrib><creatorcontrib>Hostetler, Jessicah</creatorcontrib><creatorcontrib>Fedorova, Nadia B</creatorcontrib><creatorcontrib>Proudfoot, Katie</creatorcontrib><creatorcontrib>Katzel, Dan A</creatorcontrib><creatorcontrib>Stockwell, Tim B</creatorcontrib><creatorcontrib>Ghedin, Elodie</creatorcontrib><creatorcontrib>Spiro, David J</creatorcontrib><creatorcontrib>Brown, Earl G</creatorcontrib><title>Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Adaptive evolution is characterized by positive and parallel, or repeated selection of mutations. Mouse adaptation of influenza A virus (IAV) produces virulent mutants that demonstrate positive and parallel evolution of mutations in the hemagglutinin (HA) receptor and non-structural protein 1 (NS1) interferon antagonist genes. We now present a genomic analysis of all 11 genes of 39 mouse adapted IAV variants from 10 replicate adaptation experiments. Mutations were mapped on the primary and structural maps of each protein and specific mutations were validated with respect to virulence, replication, and RNA polymerase activity. Mouse adapted (MA) variants obtained after 12 or 20-21 serial infections acquired on average 5.8 and 7.9 nonsynonymous mutations per genome of 11 genes, respectively. Among a total of 115 nonsynonymous mutations, 51 demonstrated properties of natural selection including 27 parallel mutations. The greatest degree of parallel evolution occurred in the HA receptor and ribonucleocapsid components, polymerase subunits (PB1, PB2, PA) and NP. Mutations occurred in host nuclear trafficking factor binding sites as well as sites of virus-virus protein subunit interaction for NP, NS1, HA and NA proteins. Adaptive regions included cap binding and endonuclease domains in the PB2 and PA polymerase subunits. Four mutations in NS1 resulted in loss of binding to the host cleavage and polyadenylation specificity factor (CPSF30) suggesting that a reduction in inhibition of host gene expression was being selected. The most prevalent mutations in PB2 and NP were shown to increase virulence but differed in their ability to enhance replication and demonstrated epistatic effects. Several positively selected RNA polymerase mutations demonstrated increased virulence associated with >300% enhanced polymerase activity. Adaptive mutations that control host range and virulence were identified by their repeated selection to comprise a defined model for studying IAV evolution to increased virulence in the mouse.</description><subject>Adaptation</subject><subject>Adaptive control</subject><subject>Analysis</subject><subject>Animal experimentation</subject><subject>Animals</subject><subject>Binding sites</subject><subject>Biochemistry</subject><subject>Biological response modifiers</subject><subject>Biology</subject><subject>Cell Line</subject><subject>DNA-directed RNA polymerase</subject><subject>Dogs</subject><subject>Drug resistance</subject><subject>Endonuclease</subject><subject>Epistasis</subject><subject>Evolution</subject><subject>Evolution & development</subject><subject>Evolutionary biology</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Genome, Viral - genetics</subject><subject>Genomes</subject><subject>Genomic analysis</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Hemagglutinins</subject><subject>Hepatitis</subject><subject>Host range</subject><subject>Human evolution</subject><subject>Humans</subject><subject>Immunology</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Influenza</subject><subject>Influenza A</subject><subject>Influenza A virus - genetics</subject><subject>Influenza A virus - metabolism</subject><subject>Interferon</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Mice</subject><subject>Molecular biology</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Natural selection</subject><subject>Pathogenesis</subject><subject>Polyadenylation</subject><subject>Protein binding</subject><subject>Proteins</subject><subject>Replication</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA polymerase</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><subject>Virology</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - genetics</subject><subject>Virus 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and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse</title><author>Ping, Jihui ; Keleta, Liya ; Forbes, Nicole E ; Dankar, Samar ; Stecho, William ; Tyler, Shaun ; Zhou, Yan ; Babiuk, Lorne ; Weingartl, Hana ; Halpin, Rebecca A ; Boyne, Alex ; Bera, Jayati ; Hostetler, Jessicah ; Fedorova, Nadia B ; Proudfoot, Katie ; Katzel, Dan A ; Stockwell, Tim B ; Ghedin, Elodie ; Spiro, David J ; Brown, Earl G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c757t-761ad73391426a3f06330bc1f14a5d6d57b3709910c5b17dd658b4aa792be6823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adaptation</topic><topic>Adaptive control</topic><topic>Analysis</topic><topic>Animal experimentation</topic><topic>Animals</topic><topic>Binding sites</topic><topic>Biochemistry</topic><topic>Biological response 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Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ping, Jihui</au><au>Keleta, Liya</au><au>Forbes, Nicole E</au><au>Dankar, Samar</au><au>Stecho, William</au><au>Tyler, Shaun</au><au>Zhou, Yan</au><au>Babiuk, Lorne</au><au>Weingartl, Hana</au><au>Halpin, Rebecca A</au><au>Boyne, Alex</au><au>Bera, Jayati</au><au>Hostetler, Jessicah</au><au>Fedorova, Nadia B</au><au>Proudfoot, Katie</au><au>Katzel, Dan A</au><au>Stockwell, Tim B</au><au>Ghedin, Elodie</au><au>Spiro, David J</au><au>Brown, Earl G</au><au>Zhang, Luwen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2011-06-30</date><risdate>2011</risdate><volume>6</volume><issue>6</issue><spage>e21740</spage><epage>e21740</epage><pages>e21740-e21740</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Adaptive evolution is characterized by positive and parallel, or repeated selection of mutations. Mouse adaptation of influenza A virus (IAV) produces virulent mutants that demonstrate positive and parallel evolution of mutations in the hemagglutinin (HA) receptor and non-structural protein 1 (NS1) interferon antagonist genes. We now present a genomic analysis of all 11 genes of 39 mouse adapted IAV variants from 10 replicate adaptation experiments. Mutations were mapped on the primary and structural maps of each protein and specific mutations were validated with respect to virulence, replication, and RNA polymerase activity. Mouse adapted (MA) variants obtained after 12 or 20-21 serial infections acquired on average 5.8 and 7.9 nonsynonymous mutations per genome of 11 genes, respectively. Among a total of 115 nonsynonymous mutations, 51 demonstrated properties of natural selection including 27 parallel mutations. The greatest degree of parallel evolution occurred in the HA receptor and ribonucleocapsid components, polymerase subunits (PB1, PB2, PA) and NP. Mutations occurred in host nuclear trafficking factor binding sites as well as sites of virus-virus protein subunit interaction for NP, NS1, HA and NA proteins. Adaptive regions included cap binding and endonuclease domains in the PB2 and PA polymerase subunits. Four mutations in NS1 resulted in loss of binding to the host cleavage and polyadenylation specificity factor (CPSF30) suggesting that a reduction in inhibition of host gene expression was being selected. The most prevalent mutations in PB2 and NP were shown to increase virulence but differed in their ability to enhance replication and demonstrated epistatic effects. Several positively selected RNA polymerase mutations demonstrated increased virulence associated with >300% enhanced polymerase activity. Adaptive mutations that control host range and virulence were identified by their repeated selection to comprise a defined model for studying IAV evolution to increased virulence in the mouse.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21738783</pmid><doi>10.1371/journal.pone.0021740</doi><tpages>e21740</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2011-06, Vol.6 (6), p.e21740-e21740 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1319238037 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adaptation Adaptive control Analysis Animal experimentation Animals Binding sites Biochemistry Biological response modifiers Biology Cell Line DNA-directed RNA polymerase Dogs Drug resistance Endonuclease Epistasis Evolution Evolution & development Evolutionary biology Gene expression Gene mapping Genes Genetic research Genome, Viral - genetics Genomes Genomic analysis Genomics Health aspects Hemagglutinins Hepatitis Host range Human evolution Humans Immunology Infections Infectious diseases Influenza Influenza A Influenza A virus - genetics Influenza A virus - metabolism Interferon Medical research Medicine Mice Molecular biology Mutants Mutation Natural selection Pathogenesis Polyadenylation Protein binding Proteins Replication Ribonucleic acid RNA RNA polymerase Viral Proteins - genetics Viral Proteins - metabolism Virology Virulence Virulence (Microbiology) Virulence - genetics Virus replication Viruses |
| title | Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse |
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