Variations in the Hemagglutinin of the 2009 H1N1 Pandemic Virus: Potential for Strains with Altered Virulence Phenotype?
Identifieur interne : 000D97 ( Main/Exploration ); précédent : 000D96; suivant : 000D98Variations in the Hemagglutinin of the 2009 H1N1 Pandemic Virus: Potential for Strains with Altered Virulence Phenotype?
Auteurs : Jianqiang Ye [États-Unis] ; Erin M. Sorrell [États-Unis] ; Yibin Cai [États-Unis] ; Hongxia Shao [États-Unis] ; Kemin Xu [États-Unis] ; Lindomar Pena [États-Unis] ; Danielle Hickman [États-Unis] ; Haichen Song [États-Unis] ; Matthew Angel [États-Unis] ; Rafael A. Medina [États-Unis] ; Balaji Manicassamy [États-Unis] ; Adolfo Garcia-Sastre [États-Unis] ; Daniel R. Perez [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2010.
Abstract
A novel, swine-origin influenza H1N1 virus (H1N1pdm) caused the first pandemic of the 21st century. This pandemic, although efficient in transmission, is mild in virulence. This atypical mild pandemic season has raised concerns regarding the potential of this virus to acquire additional virulence markers either through further adaptation or possibly by immune pressure in the human host. Using the mouse model we generated, within a single round of infection with A/California/04/09/H1N1 (Ca/04), a virus lethal in mice—herein referred to as mouse-adapted Ca/04 (ma-Ca/04). Five amino acid substitutions were found in the genome of ma-Ca/04: 3 in HA (D131E, S186P and A198E), 1 in PA (E298K) and 1 in NP (D101G). Reverse genetics analyses of these mutations indicate that all five mutations from ma-Ca/04 contributed to the lethal phenotype; however, the D131E and S186P mutations—which are also found in the 1918 and seasonal H1N1 viruses—in HA alone were sufficient to confer virulence of Ca/04 in mice. HI assays against H1N1pdm demonstrate that the D131E and S186P mutations caused minor antigenic changes and, likely, affected receptor binding. The rapid selection of ma-Ca/04 in mice suggests that a virus containing this constellation of amino acids might have already been present in Ca/04, likely as minor quasispecies.
Url:
DOI: 10.1371/journal.ppat.1001145
PubMed: 20976194
PubMed Central: 2954835
Affiliations:
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Sorrell</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Cai, Yibin" sort="Cai, Yibin" uniqKey="Cai Y" first="Yibin" last="Cai">Yibin Cai</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Shao, Hongxia" sort="Shao, Hongxia" uniqKey="Shao H" first="Hongxia" last="Shao">Hongxia Shao</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Xu, Kemin" sort="Xu, Kemin" uniqKey="Xu K" first="Kemin" last="Xu">Kemin Xu</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Pena, Lindomar" sort="Pena, Lindomar" uniqKey="Pena L" first="Lindomar" last="Pena">Lindomar Pena</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Hickman, Danielle" sort="Hickman, Danielle" uniqKey="Hickman D" first="Danielle" last="Hickman">Danielle Hickman</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Song, Haichen" sort="Song, Haichen" uniqKey="Song H" first="Haichen" last="Song">Haichen Song</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Synbiotics Corporation, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Synbiotics Corporation, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Angel, Matthew" sort="Angel, Matthew" uniqKey="Angel M" first="Matthew" last="Angel">Matthew Angel</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation></author><author><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Manicassamy, Balaji" sort="Manicassamy, Balaji" uniqKey="Manicassamy B" first="Balaji" last="Manicassamy">Balaji Manicassamy</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="Garcia-Sastre">Adolfo Garcia-Sastre</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Institute of Global Health and Emerging Pathogens, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Division of Infectious Diseases, Mount Sinai School of Medicine, New York, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia-Maryland Regional College of Veterinary Medicine, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></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="2010">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>A novel, swine-origin influenza H1N1 virus (H1N1pdm) caused the first pandemic of the 21<sup>st</sup> century. This pandemic, although efficient in transmission, is mild in virulence. This atypical mild pandemic season has raised concerns regarding the potential of this virus to acquire additional virulence markers either through further adaptation or possibly by immune pressure in the human host. Using the mouse model we generated, within a single round of infection with A/California/04/09/H1N1 (Ca/04), a virus lethal in mice—herein referred to as mouse-adapted Ca/04 (ma-Ca/04). Five amino acid substitutions were found in the genome of ma-Ca/04: 3 in HA (D131E, S186P and A198E), 1 in PA (E298K) and 1 in NP (D101G). Reverse genetics analyses of these mutations indicate that all five mutations from ma-Ca/04 contributed to the lethal phenotype; however, the D131E and S186P mutations—which are also found in the 1918 and seasonal H1N1 viruses—in HA alone were sufficient to confer virulence of Ca/04 in mice. HI assays against H1N1pdm demonstrate that the D131E and S186P mutations caused minor antigenic changes and, likely, affected receptor binding. The rapid selection of ma-Ca/04 in mice suggests that a virus containing this constellation of amino acids might have already been present in Ca/04, likely as minor quasispecies.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Libster, R" uniqKey="Libster R">R Libster</name></author><author><name sortKey="Bugna, J" uniqKey="Bugna J">J Bugna</name></author><author><name sortKey="Coviello, S" uniqKey="Coviello S">S Coviello</name></author><author><name sortKey="Hijano, Dr" uniqKey="Hijano D">DR Hijano</name></author><author><name sortKey="Dunaiewsky, M" uniqKey="Dunaiewsky M">M Dunaiewsky</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Louie, Jk" uniqKey="Louie J">JK Louie</name></author><author><name sortKey="Acosta, M" uniqKey="Acosta M">M Acosta</name></author><author><name sortKey="Winter, K" uniqKey="Winter K">K Winter</name></author><author><name sortKey="Jean, C" uniqKey="Jean C">C 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Bailey</name></author><author><name sortKey="Schmidt, Lm" uniqKey="Schmidt L">LM Schmidt</name></author><author><name sortKey="Hickman, Hd" uniqKey="Hickman H">HD Hickman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Munster, Vj" uniqKey="Munster V">VJ Munster</name></author><author><name sortKey="De Wit, E" uniqKey="De Wit E">E de Wit</name></author><author><name sortKey="Van Den Brand, Jm" uniqKey="Van Den Brand J">JM van den Brand</name></author><author><name sortKey="Herfst, S" uniqKey="Herfst S">S Herfst</name></author><author><name sortKey="Schrauwen, Ej" uniqKey="Schrauwen E">EJ Schrauwen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Reed, Lj" uniqKey="Reed L">LJ Reed</name></author><author><name sortKey="Muench, H" uniqKey="Muench H">H Muench</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wan, H" uniqKey="Wan H">H Wan</name></author><author><name sortKey="Sorrell, Em" uniqKey="Sorrell E">EM Sorrell</name></author><author><name sortKey="Song, H" uniqKey="Song H">H Song</name></author><author><name sortKey="Hossain, Mj" uniqKey="Hossain M">MJ Hossain</name></author><author><name sortKey="Ramirez Nieto, G" uniqKey="Ramirez Nieto G">G Ramirez-Nieto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sorrell, Em" uniqKey="Sorrell E">EM Sorrell</name></author><author><name sortKey="Wan, H" uniqKey="Wan H">H Wan</name></author><author><name sortKey="Araya, Y" uniqKey="Araya Y">Y Araya</name></author><author><name sortKey="Song, H" uniqKey="Song H">H Song</name></author><author><name sortKey="Perez, Dr" uniqKey="Perez D">DR Perez</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hoffmann, E" uniqKey="Hoffmann E">E Hoffmann</name></author><author><name sortKey="Stech, J" uniqKey="Stech J">J Stech</name></author><author><name sortKey="Guan, Y" uniqKey="Guan Y">Y Guan</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author><author><name sortKey="Perez, Dr" uniqKey="Perez D">DR Perez</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hoffmann, E" uniqKey="Hoffmann E">E Hoffmann</name></author><author><name sortKey="Krauss, S" uniqKey="Krauss S">S Krauss</name></author><author><name sortKey="Perez, D" uniqKey="Perez D">D Perez</name></author><author><name sortKey="Webby, R" uniqKey="Webby R">R Webby</name></author><author><name sortKey="Webster, Rg" uniqKey="Webster R">RG Webster</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>États-Unis</li></country><region><li>Maryland</li><li>État de New York</li></region><settlement><li>College Park (Maryland)</li></settlement><orgName><li>Université du Maryland</li></orgName></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Ye, Jianqiang" sort="Ye, Jianqiang" uniqKey="Ye J" first="Jianqiang" last="Ye">Jianqiang Ye</name></region><name sortKey="Angel, Matthew" sort="Angel, Matthew" uniqKey="Angel M" first="Matthew" last="Angel">Matthew Angel</name><name sortKey="Angel, Matthew" sort="Angel, Matthew" uniqKey="Angel M" first="Matthew" last="Angel">Matthew Angel</name><name sortKey="Cai, Yibin" sort="Cai, Yibin" uniqKey="Cai Y" first="Yibin" last="Cai">Yibin Cai</name><name sortKey="Cai, Yibin" sort="Cai, Yibin" uniqKey="Cai Y" first="Yibin" last="Cai">Yibin Cai</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="Garcia-Sastre">Adolfo Garcia-Sastre</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="Garcia-Sastre">Adolfo Garcia-Sastre</name><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="Garcia-Sastre">Adolfo Garcia-Sastre</name><name sortKey="Hickman, Danielle" sort="Hickman, Danielle" uniqKey="Hickman D" first="Danielle" last="Hickman">Danielle Hickman</name><name sortKey="Hickman, Danielle" sort="Hickman, Danielle" uniqKey="Hickman D" first="Danielle" last="Hickman">Danielle Hickman</name><name sortKey="Manicassamy, Balaji" sort="Manicassamy, Balaji" uniqKey="Manicassamy B" first="Balaji" last="Manicassamy">Balaji Manicassamy</name><name sortKey="Manicassamy, Balaji" sort="Manicassamy, Balaji" uniqKey="Manicassamy B" first="Balaji" last="Manicassamy">Balaji Manicassamy</name><name sortKey="Manicassamy, Balaji" sort="Manicassamy, Balaji" uniqKey="Manicassamy B" first="Balaji" last="Manicassamy">Balaji Manicassamy</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><name sortKey="Medina, Rafael A" sort="Medina, Rafael A" uniqKey="Medina R" first="Rafael A." last="Medina">Rafael A. Medina</name><name sortKey="Pena, Lindomar" sort="Pena, Lindomar" uniqKey="Pena L" first="Lindomar" last="Pena">Lindomar Pena</name><name sortKey="Pena, Lindomar" sort="Pena, Lindomar" uniqKey="Pena L" first="Lindomar" last="Pena">Lindomar Pena</name><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><name sortKey="Shao, Hongxia" sort="Shao, Hongxia" uniqKey="Shao H" first="Hongxia" last="Shao">Hongxia Shao</name><name sortKey="Shao, Hongxia" sort="Shao, Hongxia" uniqKey="Shao H" first="Hongxia" last="Shao">Hongxia Shao</name><name sortKey="Song, Haichen" sort="Song, Haichen" uniqKey="Song H" first="Haichen" last="Song">Haichen Song</name><name sortKey="Sorrell, Erin M" sort="Sorrell, Erin M" uniqKey="Sorrell E" first="Erin M." last="Sorrell">Erin M. Sorrell</name><name sortKey="Sorrell, Erin M" sort="Sorrell, Erin M" uniqKey="Sorrell E" first="Erin M." last="Sorrell">Erin M. Sorrell</name><name sortKey="Xu, Kemin" sort="Xu, Kemin" uniqKey="Xu K" first="Kemin" last="Xu">Kemin Xu</name><name sortKey="Xu, Kemin" sort="Xu, Kemin" uniqKey="Xu K" first="Kemin" last="Xu">Kemin Xu</name><name sortKey="Ye, Jianqiang" sort="Ye, Jianqiang" uniqKey="Ye J" first="Jianqiang" last="Ye">Jianqiang Ye</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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