SARS-CoV Pathogenesis Is Regulated by a STAT1 Dependent but a Type I, II and III Interferon Receptor Independent Mechanism
Identifieur interne : 002457 ( Main/Exploration ); précédent : 002456; suivant : 002458SARS-CoV Pathogenesis Is Regulated by a STAT1 Dependent but a Type I, II and III Interferon Receptor Independent Mechanism
Auteurs : Matthew B. Frieman [États-Unis] ; Jun Chen [États-Unis] ; Thomas E. Morrison [États-Unis] ; Alan Whitmore [États-Unis] ; William Funkhouser [États-Unis] ; Jerrold M. Ward [États-Unis] ; Elaine W. Lamirande [États-Unis] ; Anjeanette Roberts [États-Unis] ; Mark Heise [États-Unis] ; Kanta Subbarao [États-Unis] ; Ralph S. Baric [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2010.
Descripteurs français
- KwdFr :
- Analyse de profil d'expression de gènes, Animaux, Cytokines (biosynthèse), Cytométrie en flux, Expression des gènes, Facteur de transcription STAT-1 (génétique), Facteur de transcription STAT-1 (immunologie), Facteur de transcription STAT-1 (métabolisme), Femelle, Hybridation in situ, Interféron de type I (génétique), Interféron de type I (immunologie), Interféron de type I (métabolisme), Interféron gamma (génétique), Interféron gamma (immunologie), Interféron gamma (métabolisme), RT-PCR, Récepteur interféron (génétique), Récepteur interféron (immunologie), Récepteur interféron (métabolisme), Souris, Souris knockout, Syndrome respiratoire aigu sévère (génétique), Syndrome respiratoire aigu sévère (immunologie), Syndrome respiratoire aigu sévère (métabolisme), Virus du SRAS (immunologie).
- MESH :
- biosynthèse : Cytokines.
- génétique : Facteur de transcription STAT-1, Interféron de type I, Interféron gamma, Récepteur interféron, Syndrome respiratoire aigu sévère.
- immunologie : Facteur de transcription STAT-1, Interféron de type I, Interféron gamma, Récepteur interféron, Syndrome respiratoire aigu sévère, Virus du SRAS.
- métabolisme : Facteur de transcription STAT-1, Interféron de type I, Interféron gamma, Récepteur interféron, Syndrome respiratoire aigu sévère.
- Analyse de profil d'expression de gènes, Animaux, Cytométrie en flux, Expression des gènes, Femelle, Hybridation in situ, RT-PCR, Souris, Souris knockout.
English descriptors
- KwdEn :
- Animals, Cytokines (biosynthesis), Female, Flow Cytometry, Gene Expression, Gene Expression Profiling, In Situ Hybridization, Interferon Type I (genetics), Interferon Type I (immunology), Interferon Type I (metabolism), Interferon-gamma (genetics), Interferon-gamma (immunology), Interferon-gamma (metabolism), Mice, Mice, Knockout, Receptors, Interferon (genetics), Receptors, Interferon (immunology), Receptors, Interferon (metabolism), Reverse Transcriptase Polymerase Chain Reaction, SARS Virus (immunology), STAT1 Transcription Factor (genetics), STAT1 Transcription Factor (immunology), STAT1 Transcription Factor (metabolism), Severe Acute Respiratory Syndrome (genetics), Severe Acute Respiratory Syndrome (immunology), Severe Acute Respiratory Syndrome (metabolism).
- MESH :
- chemical , biosynthesis : Cytokines.
- chemical , genetics : Interferon Type I, Interferon-gamma, Receptors, Interferon, STAT1 Transcription Factor.
- chemical , immunology : Interferon Type I, Interferon-gamma, Receptors, Interferon, STAT1 Transcription Factor.
- chemical , metabolism : Interferon Type I, Interferon-gamma, Receptors, Interferon, STAT1 Transcription Factor.
- genetics : Severe Acute Respiratory Syndrome.
- immunology : SARS Virus, Severe Acute Respiratory Syndrome.
- metabolism : Severe Acute Respiratory Syndrome.
- Animals, Female, Flow Cytometry, Gene Expression, Gene Expression Profiling, In Situ Hybridization, Mice, Mice, Knockout, Reverse Transcriptase Polymerase Chain Reaction.
Abstract
Severe acute respiratory syndrome coronavirus (SARS-CoV) infection often caused severe end stage lung disease and organizing phase diffuse alveolar damage, especially in the elderly. The virus-host interactions that governed development of these acute end stage lung diseases and death are unknown. To address this question, we evaluated the role of innate immune signaling in protection from human (Urbani) and a recombinant mouse adapted SARS-CoV, designated rMA15. In contrast to most models of viral pathogenesis, infection of type I, type II or type III interferon knockout mice (129 background) with either Urbani or MA15 viruses resulted in clinical disease outcomes, including transient weight loss, denuding bronchiolitis and alveolar inflammation and recovery, identical to that seen in infection of wildtype mice. This suggests that type I, II and III interferon signaling play minor roles in regulating SARS pathogenesis in mouse models. In contrast, infection of STAT1−/− mice resulted in severe disease, high virus titer, extensive pulmonary lesions and 100% mortality by day 9 and 30 post-infection with rMA15 or Urbani viruses, respectively. Non-lethal in BALB/c mice, Urbani SARS-CoV infection in STAT1−/− mice caused disseminated infection involving the liver, spleen and other tissues after day 9. These findings demonstrated that SARS-CoV pathogenesis is regulated by a STAT1 dependent but type I, II and III interferon receptor independent, mechanism. In contrast to a well documented role in innate immunity, we propose that STAT1 also protects mice via its role as an antagonist of unrestrained cell proliferation.
Url:
DOI: 10.1371/journal.ppat.1000849
PubMed: 20386712
PubMed Central: 2851658
Affiliations:
- États-Unis
- Caroline du Nord, Maryland
- Chapel Hill (Caroline du Nord)
- Université de Caroline du Nord à Chapel Hill
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Le document en format XML
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Frieman</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation></author><author><name sortKey="Chen, Jun" sort="Chen, Jun" uniqKey="Chen J" first="Jun" last="Chen">Jun Chen</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Morrison, Thomas E" sort="Morrison, Thomas E" uniqKey="Morrison T" first="Thomas E." last="Morrison">Thomas E. Morrison</name><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation></author><author><name sortKey="Whitmore, Alan" sort="Whitmore, Alan" uniqKey="Whitmore A" first="Alan" last="Whitmore">Alan Whitmore</name><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation></author><author><name sortKey="Funkhouser, William" sort="Funkhouser, William" uniqKey="Funkhouser W" first="William" last="Funkhouser">William Funkhouser</name><affiliation wicri:level="4"><nlm:aff id="aff4"><addr-line>Department of Anatomic Pathology and Surgical Pathology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anatomic Pathology and Surgical Pathology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation></author><author><name sortKey="Ward, Jerrold M" sort="Ward, Jerrold M" uniqKey="Ward J" first="Jerrold M." last="Ward">Jerrold M. Ward</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Comparative Medicine Branch, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Comparative Medicine Branch, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Laboratory of Immunopathology, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Immunopathology, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Lamirande, Elaine W" sort="Lamirande, Elaine W" uniqKey="Lamirande E" first="Elaine W." last="Lamirande">Elaine W. Lamirande</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Roberts, Anjeanette" sort="Roberts, Anjeanette" uniqKey="Roberts A" first="Anjeanette" last="Roberts">Anjeanette Roberts</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Heise, Mark" sort="Heise, Mark" uniqKey="Heise M" first="Mark" last="Heise">Mark Heise</name><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation></author><author><name sortKey="Subbarao, Kanta" sort="Subbarao, Kanta" uniqKey="Subbarao K" first="Kanta" last="Subbarao">Kanta Subbarao</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Infectious Diseases, NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Baric, Ralph S" sort="Baric, Ralph S" uniqKey="Baric R" first="Ralph S." last="Baric">Ralph S. Baric</name><affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea><placeName><region type="state">Caroline du Nord</region><settlement type="city">Chapel Hill (Caroline du Nord)</settlement></placeName><orgName type="university">Université de Caroline du Nord à Chapel Hill</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><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Cytokines (biosynthesis)</term><term>Female</term><term>Flow Cytometry</term><term>Gene Expression</term><term>Gene Expression Profiling</term><term>In Situ Hybridization</term><term>Interferon Type I (genetics)</term><term>Interferon Type I (immunology)</term><term>Interferon Type I (metabolism)</term><term>Interferon-gamma (genetics)</term><term>Interferon-gamma (immunology)</term><term>Interferon-gamma (metabolism)</term><term>Mice</term><term>Mice, Knockout</term><term>Receptors, Interferon (genetics)</term><term>Receptors, Interferon (immunology)</term><term>Receptors, Interferon (metabolism)</term><term>Reverse Transcriptase Polymerase Chain Reaction</term><term>SARS Virus (immunology)</term><term>STAT1 Transcription Factor (genetics)</term><term>STAT1 Transcription Factor (immunology)</term><term>STAT1 Transcription Factor (metabolism)</term><term>Severe Acute Respiratory Syndrome (genetics)</term><term>Severe Acute Respiratory Syndrome (immunology)</term><term>Severe Acute Respiratory Syndrome (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Analyse de profil d'expression de gènes</term><term>Animaux</term><term>Cytokines (biosynthèse)</term><term>Cytométrie en flux</term><term>Expression des gènes</term><term>Facteur de transcription STAT-1 (génétique)</term><term>Facteur de transcription STAT-1 (immunologie)</term><term>Facteur de transcription STAT-1 (métabolisme)</term><term>Femelle</term><term>Hybridation in situ</term><term>Interféron de type I (génétique)</term><term>Interféron de type I (immunologie)</term><term>Interféron de type I (métabolisme)</term><term>Interféron gamma (génétique)</term><term>Interféron gamma (immunologie)</term><term>Interféron gamma (métabolisme)</term><term>RT-PCR</term><term>Récepteur interféron (génétique)</term><term>Récepteur interféron (immunologie)</term><term>Récepteur interféron (métabolisme)</term><term>Souris</term><term>Souris knockout</term><term>Syndrome respiratoire aigu sévère (génétique)</term><term>Syndrome respiratoire aigu sévère (immunologie)</term><term>Syndrome respiratoire aigu sévère (métabolisme)</term><term>Virus du SRAS (immunologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>Cytokines</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Interferon Type I</term><term>Interferon-gamma</term><term>Receptors, Interferon</term><term>STAT1 Transcription Factor</term></keywords><keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en"><term>Interferon Type I</term><term>Interferon-gamma</term><term>Receptors, Interferon</term><term>STAT1 Transcription Factor</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Interferon Type I</term><term>Interferon-gamma</term><term>Receptors, Interferon</term><term>STAT1 Transcription Factor</term></keywords><keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr"><term>Cytokines</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Severe Acute Respiratory Syndrome</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Facteur de transcription STAT-1</term><term>Interféron de type I</term><term>Interféron gamma</term><term>Récepteur interféron</term><term>Syndrome respiratoire aigu sévère</term></keywords><keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Facteur de transcription STAT-1</term><term>Interféron de type I</term><term>Interféron gamma</term><term>Récepteur interféron</term><term>Syndrome respiratoire aigu sévère</term><term>Virus du SRAS</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>SARS Virus</term><term>Severe Acute Respiratory Syndrome</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Severe Acute Respiratory Syndrome</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Facteur de transcription STAT-1</term><term>Interféron de type I</term><term>Interféron gamma</term><term>Récepteur interféron</term><term>Syndrome respiratoire aigu sévère</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Female</term><term>Flow Cytometry</term><term>Gene Expression</term><term>Gene Expression Profiling</term><term>In Situ Hybridization</term><term>Mice</term><term>Mice, Knockout</term><term>Reverse Transcriptase Polymerase Chain Reaction</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Analyse de profil d'expression de gènes</term><term>Animaux</term><term>Cytométrie en flux</term><term>Expression des gènes</term><term>Femelle</term><term>Hybridation in situ</term><term>RT-PCR</term><term>Souris</term><term>Souris knockout</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Severe acute respiratory syndrome coronavirus (SARS-CoV) infection often caused severe end stage lung disease and organizing phase diffuse alveolar damage, especially in the elderly. The virus-host interactions that governed development of these acute end stage lung diseases and death are unknown. To address this question, we evaluated the role of innate immune signaling in protection from human (Urbani) and a recombinant mouse adapted SARS-CoV, designated rMA15. In contrast to most models of viral pathogenesis, infection of type I, type II or type III interferon knockout mice (129 background) with either Urbani or MA15 viruses resulted in clinical disease outcomes, including transient weight loss, denuding bronchiolitis and alveolar inflammation and recovery, identical to that seen in infection of wildtype mice. This suggests that type I, II and III interferon signaling play minor roles in regulating SARS pathogenesis in mouse models. In contrast, infection of STAT1−/− mice resulted in severe disease, high virus titer, extensive pulmonary lesions and 100% mortality by day 9 and 30 post-infection with rMA15 or Urbani viruses, respectively. Non-lethal in BALB/c mice, Urbani SARS-CoV infection in STAT1−/− mice caused disseminated infection involving the liver, spleen and other tissues after day 9. These findings demonstrated that SARS-CoV pathogenesis is regulated by a STAT1 dependent but type I, II and III interferon receptor independent, mechanism. In contrast to a well documented role in innate immunity, we propose that STAT1 also protects mice via its role as an antagonist of unrestrained cell proliferation.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Donnelly, Ca" uniqKey="Donnelly C">CA Donnelly</name></author><author><name sortKey="Ghani, Ac" uniqKey="Ghani A">AC Ghani</name></author><author><name sortKey="Leung, Gm" uniqKey="Leung G">GM Leung</name></author><author><name sortKey="Hedley, Aj" uniqKey="Hedley A">AJ Hedley</name></author><author><name sortKey="Fraser, C" uniqKey="Fraser C">C Fraser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Drosten, C" uniqKey="Drosten C">C Drosten</name></author><author><name sortKey="Gunther, S" uniqKey="Gunther S">S Gunther</name></author><author><name sortKey="Preiser, W" uniqKey="Preiser W">W Preiser</name></author><author><name sortKey="Van Der Werf, S" uniqKey="Van Der Werf S">S van der 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sortKey="Mishani, E" uniqKey="Mishani E">E Mishani</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yoon, P" uniqKey="Yoon P">P Yoon</name></author><author><name sortKey="Keylock, Kt" uniqKey="Keylock K">KT Keylock</name></author><author><name sortKey="Hartman, Me" uniqKey="Hartman M">ME Hartman</name></author><author><name sortKey="Freund, Gg" uniqKey="Freund G">GG Freund</name></author><author><name sortKey="Woods, Ja" uniqKey="Woods J">JA Woods</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lau, Yl" uniqKey="Lau Y">YL Lau</name></author><author><name sortKey="Peiris, Js" uniqKey="Peiris J">JS Peiris</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Frieman, M" uniqKey="Frieman M">M Frieman</name></author><author><name sortKey="Ratia, K" uniqKey="Ratia K">K Ratia</name></author><author><name sortKey="Johnston, Re" uniqKey="Johnston R">RE Johnston</name></author><author><name sortKey="Mesecar, Ad" uniqKey="Mesecar A">AD Mesecar</name></author><author><name sortKey="Baric, Rs" uniqKey="Baric R">RS Baric</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nicholls, Jm" uniqKey="Nicholls J">JM Nicholls</name></author><author><name sortKey="Butany, J" uniqKey="Butany J">J Butany</name></author><author><name sortKey="Poon, Ll" uniqKey="Poon L">LL Poon</name></author><author><name sortKey="Chan, Kh" uniqKey="Chan K">KH Chan</name></author><author><name sortKey="Beh, Sl" uniqKey="Beh S">SL Beh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chan Yeung, M" uniqKey="Chan Yeung M">M Chan-Yeung</name></author><author><name sortKey="Xu, Rh" uniqKey="Xu R">RH Xu</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>États-Unis</li></country><region><li>Caroline du Nord</li><li>Maryland</li></region><settlement><li>Chapel Hill (Caroline du Nord)</li></settlement><orgName><li>Université de Caroline du Nord à Chapel Hill</li></orgName></list><tree><country name="États-Unis"><region name="Caroline du Nord"><name sortKey="Frieman, Matthew B" sort="Frieman, Matthew B" uniqKey="Frieman M" first="Matthew B." last="Frieman">Matthew B. Frieman</name></region><name sortKey="Baric, Ralph S" sort="Baric, Ralph S" uniqKey="Baric R" first="Ralph S." last="Baric">Ralph S. Baric</name><name sortKey="Baric, Ralph S" sort="Baric, Ralph S" uniqKey="Baric R" first="Ralph S." last="Baric">Ralph S. Baric</name><name sortKey="Chen, Jun" sort="Chen, Jun" uniqKey="Chen J" first="Jun" last="Chen">Jun Chen</name><name sortKey="Funkhouser, William" sort="Funkhouser, William" uniqKey="Funkhouser W" first="William" last="Funkhouser">William Funkhouser</name><name sortKey="Heise, Mark" sort="Heise, Mark" uniqKey="Heise M" first="Mark" last="Heise">Mark Heise</name><name sortKey="Lamirande, Elaine W" sort="Lamirande, Elaine W" uniqKey="Lamirande E" first="Elaine W." last="Lamirande">Elaine W. Lamirande</name><name sortKey="Morrison, Thomas E" sort="Morrison, Thomas E" uniqKey="Morrison T" first="Thomas E." last="Morrison">Thomas E. Morrison</name><name sortKey="Roberts, Anjeanette" sort="Roberts, Anjeanette" uniqKey="Roberts A" first="Anjeanette" last="Roberts">Anjeanette Roberts</name><name sortKey="Subbarao, Kanta" sort="Subbarao, Kanta" uniqKey="Subbarao K" first="Kanta" last="Subbarao">Kanta Subbarao</name><name sortKey="Ward, Jerrold M" sort="Ward, Jerrold M" uniqKey="Ward J" first="Jerrold M." last="Ward">Jerrold M. Ward</name><name sortKey="Ward, Jerrold M" sort="Ward, Jerrold M" uniqKey="Ward J" first="Jerrold M." last="Ward">Jerrold M. Ward</name><name sortKey="Whitmore, Alan" sort="Whitmore, Alan" uniqKey="Whitmore A" first="Alan" last="Whitmore">Alan Whitmore</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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