Tissue tropisms opt for transmissible reassortants during avian and swine influenza A virus co-infection in swine
Identifieur interne : 000F39 ( Ncbi/Merge ); précédent : 000F38; suivant : 000F40Tissue tropisms opt for transmissible reassortants during avian and swine influenza A virus co-infection in swine
Auteurs : Xiaojian Zhang [États-Unis] ; Hailiang Sun [États-Unis, République populaire de Chine] ; Fred L. Cunningham [États-Unis] ; Lei Li [États-Unis] ; Katie Hanson-Dorr [États-Unis] ; Matthew W. Hopken [États-Unis] ; Jim Cooley [États-Unis] ; Li-Ping Long [États-Unis] ; John A. Baroch [États-Unis] ; Tao Li [États-Unis] ; Brandon S. Schmit [États-Unis] ; Xiaoxu Lin [États-Unis] ; Alicia K. Olivier [États-Unis] ; Richard G. Jarman [États-Unis] ; Thomas J. Deliberto [États-Unis] ; Xiu-Feng Wan [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2018.
Abstract
Genetic reassortment between influenza A viruses (IAVs) facilitate emergence of pandemic strains, and swine are proposed as a “mixing vessel” for generating reassortants of avian and mammalian IAVs that could be of risk to mammals, including humans. However, how a transmissible reassortant emerges in swine are not well understood. Genomic analyses of 571 isolates recovered from nasal wash samples and respiratory tract tissues of a group of co-housed pigs (influenza-seronegative, avian H1N1 IAV–infected, and swine H3N2 IAV–infected pigs) identified 30 distinct genotypes of reassortants. Viruses recovered from lower respiratory tract tissues had the largest genomic diversity, and those recovered from turbinates and nasal wash fluids had the least. Reassortants from lower respiratory tracts had the largest variations in growth kinetics in respiratory tract epithelial cells, and the cold temperature in swine nasal cells seemed to select the type of reassortant viruses shed by the pigs. One reassortant in nasal wash samples was consistently identified in upper, middle, and lower respiratory tract tissues, and it was confirmed to be transmitted efficiently between pigs. Study findings suggest that, during mixed infections of avian and swine IAVs, genetic reassortments are likely to occur in the lower respiratory track, and tissue tropism is an important factor selecting for a transmissible reassortant.
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DOI: 10.1371/journal.ppat.1007417
PubMed: 30507946
PubMed Central: 6292640
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Cunningham</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Mississippi Field Station, National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Mississippi Field Station, National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Li, Lei" sort="Li, Lei" uniqKey="Li L" first="Lei" last="Li">Lei Li</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Hanson Dorr, Katie" sort="Hanson Dorr, Katie" uniqKey="Hanson Dorr K" first="Katie" last="Hanson-Dorr">Katie Hanson-Dorr</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Mississippi Field Station, National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Mississippi Field Station, National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Hopken, Matthew W" sort="Hopken, Matthew W" uniqKey="Hopken M" first="Matthew W." last="Hopken">Matthew W. Hopken</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado State, Colorado, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado State, Colorado</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation></author><author><name sortKey="Cooley, Jim" sort="Cooley, Jim" uniqKey="Cooley J" first="Jim" last="Cooley">Jim Cooley</name><affiliation wicri:level="2"><nlm:aff id="aff006"><addr-line>Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Long, Li Ping" sort="Long, Li Ping" uniqKey="Long L" first="Li-Ping" last="Long">Li-Ping Long</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Baroch, John A" sort="Baroch, John A" uniqKey="Baroch J" first="John A." last="Baroch">John A. Baroch</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation></author><author><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><affiliation wicri:level="2"><nlm:aff id="aff007"><addr-line>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Schmit, Brandon S" sort="Schmit, Brandon S" uniqKey="Schmit B" first="Brandon S." last="Schmit">Brandon S. Schmit</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation></author><author><name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name><affiliation wicri:level="2"><nlm:aff id="aff007"><addr-line>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Olivier, Alicia K" sort="Olivier, Alicia K" uniqKey="Olivier A" first="Alicia K." last="Olivier">Alicia K. Olivier</name><affiliation wicri:level="2"><nlm:aff id="aff006"><addr-line>Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author><author><name sortKey="Jarman, Richard G" sort="Jarman, Richard G" uniqKey="Jarman R" first="Richard G." last="Jarman">Richard G. Jarman</name><affiliation wicri:level="2"><nlm:aff id="aff007"><addr-line>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Deliberto, Thomas J" sort="Deliberto, Thomas J" uniqKey="Deliberto T" first="Thomas J." last="Deliberto">Thomas J. Deliberto</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado</wicri:regionArea><placeName><region type="state">Colorado</region></placeName></affiliation></author><author><name sortKey="Wan, Xiu Feng" sort="Wan, Xiu Feng" uniqKey="Wan X" first="Xiu-Feng" last="Wan">Xiu-Feng Wan</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi</wicri:regionArea><placeName><region type="state">État du Mississippi</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Genetic reassortment between influenza A viruses (IAVs) facilitate emergence of pandemic strains, and swine are proposed as a “mixing vessel” for generating reassortants of avian and mammalian IAVs that could be of risk to mammals, including humans. However, how a transmissible reassortant emerges in swine are not well understood. Genomic analyses of 571 isolates recovered from nasal wash samples and respiratory tract tissues of a group of co-housed pigs (influenza-seronegative, avian H1N1 IAV–infected, and swine H3N2 IAV–infected pigs) identified 30 distinct genotypes of reassortants. Viruses recovered from lower respiratory tract tissues had the largest genomic diversity, and those recovered from turbinates and nasal wash fluids had the least. Reassortants from lower respiratory tracts had the largest variations in growth kinetics in respiratory tract epithelial cells, and the cold temperature in swine nasal cells seemed to select the type of reassortant viruses shed by the pigs. One reassortant in nasal wash samples was consistently identified in upper, middle, and lower respiratory tract tissues, and it was confirmed to be transmitted efficiently between pigs. Study findings suggest that, during mixed infections of avian and swine IAVs, genetic reassortments are likely to occur in the lower respiratory track, and tissue tropism is an important factor selecting for a transmissible reassortant.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Tong, S" uniqKey="Tong S">S Tong</name></author><author><name sortKey="Li, Y" uniqKey="Li Y">Y Li</name></author><author><name sortKey="Rivailler, P" uniqKey="Rivailler P">P Rivailler</name></author><author><name sortKey="Conrardy, C" uniqKey="Conrardy C">C Conrardy</name></author><author><name sortKey="Castillo, Da" uniqKey="Castillo D">DA Castillo</name></author><author><name sortKey="Chen, Lm" uniqKey="Chen L">LM Chen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tong, S" uniqKey="Tong S">S Tong</name></author><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Li, Y" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plospath</journal-id><journal-title-group><journal-title>PLoS Pathogens</journal-title></journal-title-group><issn pub-type="ppub">1553-7366</issn><issn pub-type="epub">1553-7374</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30507946</article-id><article-id pub-id-type="pmc">6292640</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1007417</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-18-01472</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Eukaryota</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Mammals</subject><subj-group><subject>Swine</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Eukaryota</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Birds</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Zoonoses</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Tropism</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Animal Genetics</subject><subj-group><subject>Bird Genetics</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Viral Diseases</subject><subj-group><subject>Influenza</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Tissue tropisms opt for transmissible reassortants during avian and swine influenza A virus co-infection in swine</article-title><alt-title alt-title-type="running-head">Reassortment of avian and swine 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contrib-id-type="orcid">http://orcid.org/0000-0001-6265-4622</contrib-id><name><surname>Baroch</surname><given-names>John A.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Tao</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-2313-7558</contrib-id><name><surname>Schmit</surname><given-names>Brandon S.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Xiaoxu</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Olivier</surname><given-names>Alicia K.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jarman</surname><given-names>Richard G.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1115-1472</contrib-id><name><surname>DeLiberto</surname><given-names>Thomas J.</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff004"><sup>4</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-2629-9234</contrib-id><name><surname>Wan</surname><given-names>Xiu-Feng</given-names></name><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong, China</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Mississippi Field Station, National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Starkville, Mississippi State, Mississippi, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>National Wildlife Research Center, Wildlife Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, United States of America</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado State, Colorado, United States of America</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Starkville, Mississippi State, Mississippi, United States of America</addr-line></aff><aff id="aff007"><label>7</label><addr-line>Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Lowen</surname><given-names>Anice C.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Emory University School of Medicine, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>Thomas.J.DeLiberto@aphis.usda.gov</email> (TD); <email>wan@cvm.msstate.edu</email> (XFW)</corresp></author-notes><pub-date pub-type="epub"><day>3</day><month>12</month><year>2018</year></pub-date><pub-date pub-type="collection"><month>12</month><year>2018</year></pub-date><volume>14</volume><issue>12</issue><elocation-id>e1007417</elocation-id><history><date date-type="received"><day>24</day><month>7</month><year>2018</year></date><date date-type="accepted"><day>18</day><month>10</month><year>2018</year></date></history><permissions><license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/"><license-p>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 <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">Creative Commons CC0</ext-link> public domain dedication.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="ppat.1007417.pdf"></self-uri><abstract><p>Genetic reassortment between influenza A viruses (IAVs) facilitate emergence of pandemic strains, and swine are proposed as a “mixing vessel” for generating reassortants of avian and mammalian IAVs that could be of risk to mammals, including humans. However, how a transmissible reassortant emerges in swine are not well understood. Genomic analyses of 571 isolates recovered from nasal wash samples and respiratory tract tissues of a group of co-housed pigs (influenza-seronegative, avian H1N1 IAV–infected, and swine H3N2 IAV–infected pigs) identified 30 distinct genotypes of reassortants. Viruses recovered from lower respiratory tract tissues had the largest genomic diversity, and those recovered from turbinates and nasal wash fluids had the least. Reassortants from lower respiratory tracts had the largest variations in growth kinetics in respiratory tract epithelial cells, and the cold temperature in swine nasal cells seemed to select the type of reassortant viruses shed by the pigs. One reassortant in nasal wash samples was consistently identified in upper, middle, and lower respiratory tract tissues, and it was confirmed to be transmitted efficiently between pigs. Study findings suggest that, during mixed infections of avian and swine IAVs, genetic reassortments are likely to occur in the lower respiratory track, and tissue tropism is an important factor selecting for a transmissible reassortant.</p></abstract><abstract abstract-type="summary"><title>Author summary</title><p>Genetic reassortments between avian and swine influenza viruses are likely to occur in the swine lower respiratory track, and tissue tropism is an important factor selecting for a transmissible reassortant; determination of tissue tropisms for potential reassortants between contemporary avian and swine influenza viruses would help identify transmissible reassortants with public health risks.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000199</institution-id><institution>U.S. Department of Agriculture</institution></institution-wrap></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-2629-9234</contrib-id><name><surname>Wan</surname><given-names>Xiu-Feng</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>R21AI135820</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-2629-9234</contrib-id><name><surname>Wan</surname><given-names>Xiu-Feng</given-names></name></principal-award-recipient></award-group><funding-statement>This study was supported by the U.S. Department of Agriculture and the National Institutes of Health (NIH) [grant number R21AI135820]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="0"></table-count><page-count count="22"></page-count></counts><custom-meta-group><custom-meta><meta-name>PLOS Publication Stage</meta-name><meta-value>vor-update-to-uncorrected-proof</meta-value></custom-meta><custom-meta><meta-name>Publication Update</meta-name><meta-value>2018-12-13</meta-value></custom-meta><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>The sequence of A/swine/Texas/A01104013/2012 (H3N2) and A/mallard/Wisconsin/A00751454/2009 (H1N1) viruses are available from Genbank under the accession numbers JX280447 to JX280454 and MH879773 to MH879780. All other relevant data are included in the main text of this paper or the Supporting Information files associated with this paper.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>The sequence of A/swine/Texas/A01104013/2012 (H3N2) and A/mallard/Wisconsin/A00751454/2009 (H1N1) viruses are available from Genbank under the accession numbers JX280447 to JX280454 and MH879773 to MH879780. All other relevant data are included in the main text of this paper or the Supporting Information files associated with this paper.</p></notes></front></pmc><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Colorado</li><li>Maryland</li><li>État du Mississippi</li></region></list><tree><country name="États-Unis"><region name="État du Mississippi"><name sortKey="Zhang, Xiaojian" sort="Zhang, Xiaojian" uniqKey="Zhang X" first="Xiaojian" last="Zhang">Xiaojian Zhang</name></region><name sortKey="Baroch, John A" sort="Baroch, John A" uniqKey="Baroch J" first="John A." last="Baroch">John A. Baroch</name><name sortKey="Cooley, Jim" sort="Cooley, Jim" uniqKey="Cooley J" first="Jim" last="Cooley">Jim Cooley</name><name sortKey="Cunningham, Fred L" sort="Cunningham, Fred L" uniqKey="Cunningham F" first="Fred L." last="Cunningham">Fred L. Cunningham</name><name sortKey="Deliberto, Thomas J" sort="Deliberto, Thomas J" uniqKey="Deliberto T" first="Thomas J." last="Deliberto">Thomas J. Deliberto</name><name sortKey="Hanson Dorr, Katie" sort="Hanson Dorr, Katie" uniqKey="Hanson Dorr K" first="Katie" last="Hanson-Dorr">Katie Hanson-Dorr</name><name sortKey="Hopken, Matthew W" sort="Hopken, Matthew W" uniqKey="Hopken M" first="Matthew W." last="Hopken">Matthew W. Hopken</name><name sortKey="Hopken, Matthew W" sort="Hopken, Matthew W" uniqKey="Hopken M" first="Matthew W." last="Hopken">Matthew W. Hopken</name><name sortKey="Jarman, Richard G" sort="Jarman, Richard G" uniqKey="Jarman R" first="Richard G." last="Jarman">Richard G. Jarman</name><name sortKey="Li, Lei" sort="Li, Lei" uniqKey="Li L" first="Lei" last="Li">Lei Li</name><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name><name sortKey="Long, Li Ping" sort="Long, Li Ping" uniqKey="Long L" first="Li-Ping" last="Long">Li-Ping Long</name><name sortKey="Olivier, Alicia K" sort="Olivier, Alicia K" uniqKey="Olivier A" first="Alicia K." last="Olivier">Alicia K. Olivier</name><name sortKey="Schmit, Brandon S" sort="Schmit, Brandon S" uniqKey="Schmit B" first="Brandon S." last="Schmit">Brandon S. Schmit</name><name sortKey="Sun, Hailiang" sort="Sun, Hailiang" uniqKey="Sun H" first="Hailiang" last="Sun">Hailiang Sun</name><name sortKey="Wan, Xiu Feng" sort="Wan, Xiu Feng" uniqKey="Wan X" first="Xiu-Feng" last="Wan">Xiu-Feng Wan</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Sun, Hailiang" sort="Sun, Hailiang" uniqKey="Sun H" first="Hailiang" last="Sun">Hailiang Sun</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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