A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance
Identifieur interne : 000410 ( Pmc/Checkpoint ); précédent : 000409; suivant : 000411A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance
Auteurs : Jacqueline Smith [Royaume-Uni] ; Nikki Smith [Royaume-Uni] ; Le Yu [Royaume-Uni] ; Ian R. Paton [Royaume-Uni] ; Maria Weronika Gutowska [Royaume-Uni] ; Heather L. Forrest [États-Unis] ; Angela F. Danner [États-Unis] ; J. Patrick Seiler [États-Unis] ; Paul Digard [Royaume-Uni] ; Robert G. Webster [États-Unis] ; David W. Burt [Royaume-Uni]Source :
- BMC Genomics [ 1471-2164 ] ; 2015.
Abstract
Chickens are susceptible to infection with a limited number of Influenza A viruses and are a potential source of a human influenza pandemic. In particular, H5 and H7 haemagglutinin subtypes can evolve from low to highly pathogenic strains in gallinaceous poultry. Ducks on the other hand are a natural reservoir for these viruses and are able to withstand most avian influenza strains.
Transcriptomic sequencing of lung and ileum tissue samples from birds infected with high (H5N1) and low (H5N2) pathogenic influenza viruses has allowed us to compare the early host response to these infections in both these species. Chickens (but not ducks) lack the intracellular receptor for viral ssRNA,
Taken together these results support a model where the IFITM123 protein family and RIG-I all play a crucial role in the tolerance of ducks to highly pathogenic and low pathogenic strains of avian influenza viruses when compared to the chicken.
The online version of this article (doi:10.1186/s12864-015-1778-8) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12864-015-1778-8
PubMed: 26238195
PubMed Central: 4523026
Affiliations:
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Danner</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Seiler, J Patrick" sort="Seiler, J Patrick" uniqKey="Seiler J" first="J. Patrick" last="Seiler">J. Patrick Seiler</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Digard, Paul" sort="Digard, Paul" uniqKey="Digard P" first="Paul" last="Digard">Paul Digard</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Webster, Robert G" sort="Webster, Robert G" uniqKey="Webster R" first="Robert G." last="Webster">Robert G. 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Burt</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26238195</idno><idno type="pmc">4523026</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4523026</idno><idno type="RBID">PMC:4523026</idno><idno type="doi">10.1186/s12864-015-1778-8</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000171</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000171</idno><idno type="wicri:Area/Pmc/Curation">000171</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000171</idno><idno type="wicri:Area/Pmc/Checkpoint">000410</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000410</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance</title><author><name sortKey="Smith, Jacqueline" sort="Smith, Jacqueline" uniqKey="Smith J" first="Jacqueline" last="Smith">Jacqueline Smith</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Smith, Nikki" sort="Smith, Nikki" uniqKey="Smith N" first="Nikki" last="Smith">Nikki Smith</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Yu, Le" sort="Yu, Le" uniqKey="Yu L" first="Le" last="Yu">Le Yu</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Paton, Ian R" sort="Paton, Ian R" uniqKey="Paton I" first="Ian R." last="Paton">Ian R. Paton</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Gutowska, Maria Weronika" sort="Gutowska, Maria Weronika" uniqKey="Gutowska M" first="Maria Weronika" last="Gutowska">Maria Weronika Gutowska</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Forrest, Heather L" sort="Forrest, Heather L" uniqKey="Forrest H" first="Heather L." last="Forrest">Heather L. Forrest</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Danner, Angela F" sort="Danner, Angela F" uniqKey="Danner A" first="Angela F." last="Danner">Angela F. Danner</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Seiler, J Patrick" sort="Seiler, J Patrick" uniqKey="Seiler J" first="J. Patrick" last="Seiler">J. Patrick Seiler</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Digard, Paul" sort="Digard, Paul" uniqKey="Digard P" first="Paul" last="Digard">Paul Digard</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author><author><name sortKey="Webster, Robert G" sort="Webster, Robert G" uniqKey="Webster R" first="Robert G." last="Webster">Robert G. Webster</name><affiliation wicri:level="2"><nlm:aff id="Aff2">St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis</wicri:cityArea></affiliation></author><author><name sortKey="Burt, David W" sort="Burt, David W" uniqKey="Burt D" first="David W." last="Burt">David W. Burt</name><affiliation wicri:level="4"><nlm:aff id="Aff1">The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</nlm:aff><orgName type="university">Université d'Édimbourg</orgName><country>Royaume-Uni</country><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName></affiliation></author></analytic><series><title level="j">BMC Genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Chickens are susceptible to infection with a limited number of Influenza A viruses and are a potential source of a human influenza pandemic. In particular, H5 and H7 haemagglutinin subtypes can evolve from low to highly pathogenic strains in gallinaceous poultry. Ducks on the other hand are a natural reservoir for these viruses and are able to withstand most avian influenza strains.</p></sec><sec><title>Results</title><p>Transcriptomic sequencing of lung and ileum tissue samples from birds infected with high (H5N1) and low (H5N2) pathogenic influenza viruses has allowed us to compare the early host response to these infections in both these species. Chickens (but not ducks) lack the intracellular receptor for viral ssRNA, <italic>RIG-I</italic> and the gene for an important RIG-I binding protein, RNF135. These differences in gene content partly explain the differences in host responses to low pathogenic and highly pathogenic avian influenza virus in chicken and ducks. We reveal very different patterns of expression of members of the interferon-induced transmembrane protein (<italic>IFITM</italic>) gene family in ducks and chickens. In ducks, <italic>IFITM1, 2</italic> and <italic>3</italic> are strongly up regulated in response to highly pathogenic avian influenza, where little response is seen in chickens. Clustering of gene expression profiles suggests IFITM1 and 2 have an anti-viral response and IFITM3 may restrict avian influenza virus through cell membrane fusion. We also show, through molecular phylogenetic analyses, that avian <italic>IFITM1</italic> and <italic>IFITM3</italic> genes have been subject to both episodic and pervasive positive selection at specific codons. In particular, avian <italic>IFITM1</italic> showed evidence of positive selection in the duck lineage at sites known to restrict influenza virus infection.</p></sec><sec><title>Conclusions</title><p>Taken together these results support a model where the IFITM123 protein family and RIG-I all play a crucial role in the tolerance of ducks to highly pathogenic and low pathogenic strains of avian influenza viruses when compared to the chicken.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12864-015-1778-8) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Alexander, Dj" uniqKey="Alexander D">DJ Alexander</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vanderven, Ha" uniqKey="Vanderven H">HA Vanderven</name></author><author><name sortKey="Petkau, K" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Genomics</journal-id><journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id><journal-title-group><journal-title>BMC Genomics</journal-title></journal-title-group><issn pub-type="epub">1471-2164</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26238195</article-id><article-id pub-id-type="pmc">4523026</article-id><article-id pub-id-type="publisher-id">1778</article-id><article-id pub-id-type="doi">10.1186/s12864-015-1778-8</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes" equal-contrib="yes"><name><surname>Smith</surname><given-names>Jacqueline</given-names></name><address><email>Jacqueline.smith@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Smith</surname><given-names>Nikki</given-names></name><address><email>Nikki.smith@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Yu</surname><given-names>Le</given-names></name><address><email>Le.yu@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Paton</surname><given-names>Ian R.</given-names></name><address><email>Bob.paton@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Gutowska</surname><given-names>Maria Weronika</given-names></name><address><email>MW.Gutowska@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Forrest</surname><given-names>Heather L.</given-names></name><address><email>Heather.Forrest@stjude.org</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Danner</surname><given-names>Angela F.</given-names></name><address><email>Angela.Danner@stjude.org</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Seiler</surname><given-names>J. Patrick</given-names></name><address><email>Jon.Seiler@stjude.org</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Digard</surname><given-names>Paul</given-names></name><address><email>Paul.digard@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Webster</surname><given-names>Robert G.</given-names></name><address><email>Robert.Webster@STJUDE.ORG</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="yes"><name><surname>Burt</surname><given-names>David W.</given-names></name><address><email>Dave.burt@roslin.ed.ac.uk</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1"><label></label>The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG UK</aff><aff id="Aff2"><label></label>St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis, TN 38105 USA</aff></contrib-group><pub-date pub-type="epub"><day>4</day><month>8</month><year>2015</year></pub-date><pub-date pub-type="pmc-release"><day>4</day><month>8</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>16</volume><issue>1</issue><elocation-id>574</elocation-id><history><date date-type="received"><day>26</day><month>8</month><year>2014</year></date><date date-type="accepted"><day>14</day><month>7</month><year>2015</year></date></history><permissions><copyright-statement>© Smith et al. 2015</copyright-statement><license license-type="open-access"><license-p><bold>Open Access</bold> This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p>Chickens are susceptible to infection with a limited number of Influenza A viruses and are a potential source of a human influenza pandemic. In particular, H5 and H7 haemagglutinin subtypes can evolve from low to highly pathogenic strains in gallinaceous poultry. Ducks on the other hand are a natural reservoir for these viruses and are able to withstand most avian influenza strains.</p></sec><sec><title>Results</title><p>Transcriptomic sequencing of lung and ileum tissue samples from birds infected with high (H5N1) and low (H5N2) pathogenic influenza viruses has allowed us to compare the early host response to these infections in both these species. Chickens (but not ducks) lack the intracellular receptor for viral ssRNA, <italic>RIG-I</italic> and the gene for an important RIG-I binding protein, RNF135. These differences in gene content partly explain the differences in host responses to low pathogenic and highly pathogenic avian influenza virus in chicken and ducks. We reveal very different patterns of expression of members of the interferon-induced transmembrane protein (<italic>IFITM</italic>) gene family in ducks and chickens. In ducks, <italic>IFITM1, 2</italic> and <italic>3</italic> are strongly up regulated in response to highly pathogenic avian influenza, where little response is seen in chickens. Clustering of gene expression profiles suggests IFITM1 and 2 have an anti-viral response and IFITM3 may restrict avian influenza virus through cell membrane fusion. We also show, through molecular phylogenetic analyses, that avian <italic>IFITM1</italic> and <italic>IFITM3</italic> genes have been subject to both episodic and pervasive positive selection at specific codons. In particular, avian <italic>IFITM1</italic> showed evidence of positive selection in the duck lineage at sites known to restrict influenza virus infection.</p></sec><sec><title>Conclusions</title><p>Taken together these results support a model where the IFITM123 protein family and RIG-I all play a crucial role in the tolerance of ducks to highly pathogenic and low pathogenic strains of avian influenza viruses when compared to the chicken.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12864-015-1778-8) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Avian influenza</kwd><kwd>H5N1</kwd><kwd>H5N2</kwd><kwd>Duck</kwd><kwd>Chicken</kwd><kwd>Pathogenicity</kwd><kwd>Interferon-induced transmembrane proteins</kwd><kwd>Evolution and gene expression profiles</kwd></kwd-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2015</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>Royaume-Uni</li><li>États-Unis</li></country><region><li>Tennessee</li><li>Écosse</li></region><settlement><li>Édimbourg</li></settlement><orgName><li>Université d'Édimbourg</li></orgName></list><tree><country name="Royaume-Uni"><region name="Écosse"><name sortKey="Smith, Jacqueline" sort="Smith, Jacqueline" uniqKey="Smith J" first="Jacqueline" last="Smith">Jacqueline Smith</name></region><name sortKey="Burt, David W" sort="Burt, David W" uniqKey="Burt D" first="David W." last="Burt">David W. Burt</name><name sortKey="Digard, Paul" sort="Digard, Paul" uniqKey="Digard P" first="Paul" last="Digard">Paul Digard</name><name sortKey="Gutowska, Maria Weronika" sort="Gutowska, Maria Weronika" uniqKey="Gutowska M" first="Maria Weronika" last="Gutowska">Maria Weronika Gutowska</name><name sortKey="Paton, Ian R" sort="Paton, Ian R" uniqKey="Paton I" first="Ian R." last="Paton">Ian R. Paton</name><name sortKey="Smith, Nikki" sort="Smith, Nikki" uniqKey="Smith N" first="Nikki" last="Smith">Nikki Smith</name><name sortKey="Yu, Le" sort="Yu, Le" uniqKey="Yu L" first="Le" last="Yu">Le Yu</name></country><country name="États-Unis"><region name="Tennessee"><name sortKey="Forrest, Heather L" sort="Forrest, Heather L" uniqKey="Forrest H" first="Heather L." last="Forrest">Heather L. Forrest</name></region><name sortKey="Danner, Angela F" sort="Danner, Angela F" uniqKey="Danner A" first="Angela F." last="Danner">Angela F. Danner</name><name sortKey="Seiler, J Patrick" sort="Seiler, J Patrick" uniqKey="Seiler J" first="J. Patrick" last="Seiler">J. Patrick Seiler</name><name sortKey="Webster, Robert G" sort="Webster, Robert G" uniqKey="Webster R" first="Robert G." last="Webster">Robert G. Webster</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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