Implication of Inflammatory Macrophages, Nuclear Receptors, and Interferon Regulatory Factors in Increased Virulence of Pandemic 2009 H1N1 Influenza A Virus after Host Adaptation
Identifieur interne : 000589 ( PascalFrancis/Checkpoint ); précédent : 000588; suivant : 000590Implication of Inflammatory Macrophages, Nuclear Receptors, and Interferon Regulatory Factors in Increased Virulence of Pandemic 2009 H1N1 Influenza A Virus after Host Adaptation
Auteurs : Laurence Josset [États-Unis] ; Jessica A. Belser [États-Unis] ; Mary J. Pantin-Jackwood [États-Unis] ; Jean H. Chang [États-Unis] ; Stewart T. Chang [États-Unis] ; Sarah E. Belisle [États-Unis] ; Terrence M. Tumpey [États-Unis] ; Michael G. Katze [États-Unis]Source :
- Journal of virology [ 0022-538X ] ; 2012.
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Abstract
While pandemic 2009 H1N1 influenza A viruses were responsible for numerous severe infections in humans, these viruses do not typically cause corresponding severe disease in mammalian models. However, the generation of a virulent 2009 H1N1 virus following serial lung passage in mice has allowed for the modeling of human lung pathology in this species. Genetic determinants of mouse-adapted 2009 H1N1 viral pathogenicity have been identified, but the molecular and signaling characteristics of the host response following infection with this adapted virus have not been described. Here we compared the gene expression response following infection of mice with A/CA/04/2009 (CA/04) or the virulent mouse-adapted strain (MA-CA/04). Microarray analysis revealed that increased pathogenicity of MA-CA/04 was associated with the following: (i) an early and sustained inflammatory and interferon response that could be driven in part by interferon regulatory factors (IRFs) and increased NF-KB activation, as well as inhibition of the negative regulator TRIM24, (ii) early and persistent infiltration of immune cells, including inflammatory macrophages, and (iii) the absence of activation of lipid metabolism later in infection, which may be mediated by inhibition of nuclear receptors, including PPARG and HNF1A and -4A, with proinflammatory consequences. Further investigation of these signatures in the host response to other H1N1 viruses of various pathogenicities confirmed their general relevance for virulence of influenza virus and suggested that lung response to MA-CA/04 virus was similar to that following infection with lethal H1N1 r1918 influenza virus. This study links differential activation of IRFs, nuclear receptors, and macrophage infiltration with influenza virulence in vivo.
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Chang</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Belisle, Sarah E" sort="Belisle, Sarah E" uniqKey="Belisle S" first="Sarah E." last="Belisle">Sarah E. 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Tumpey</name><affiliation wicri:level="2"><inist:fA14 i1="02"><s1>Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention</s1><s2>Atlanta, Georgia</s2><s3>USA</s3><sZ>2 aut.</sZ><sZ>7 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Katze, Michael G" sort="Katze, Michael G" uniqKey="Katze M" first="Michael G." last="Katze">Michael G. Katze</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">INIST</idno><idno type="inist">12-0269098</idno><date when="2012">2012</date><idno type="stanalyst">PASCAL 12-0269098 INIST</idno><idno type="RBID">Pascal:12-0269098</idno><idno type="wicri:Area/PascalFrancis/Corpus">000611</idno><idno type="wicri:Area/PascalFrancis/Curation">001827</idno><idno type="wicri:Area/PascalFrancis/Checkpoint">000589</idno><idno type="wicri:explorRef" wicri:stream="PascalFrancis" wicri:step="Checkpoint">000589</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a">Implication of Inflammatory Macrophages, Nuclear Receptors, and Interferon Regulatory Factors in Increased Virulence of Pandemic 2009 H1N1 Influenza A Virus after Host Adaptation</title><author><name sortKey="Josset, Laurence" sort="Josset, Laurence" uniqKey="Josset L" first="Laurence" last="Josset">Laurence Josset</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Belser, Jessica A" sort="Belser, Jessica A" uniqKey="Belser J" first="Jessica A." last="Belser">Jessica A. Belser</name><affiliation wicri:level="2"><inist:fA14 i1="02"><s1>Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention</s1><s2>Atlanta, Georgia</s2><s3>USA</s3><sZ>2 aut.</sZ><sZ>7 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Pantin Jackwood, Mary J" sort="Pantin Jackwood, Mary J" uniqKey="Pantin Jackwood M" first="Mary J." last="Pantin-Jackwood">Mary J. Pantin-Jackwood</name><affiliation wicri:level="2"><inist:fA14 i1="03"><s1>Southeast Poultry Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture</s1><s2>Athens, GA</s2><s3>USA</s3><sZ>3 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Chang, Jean H" sort="Chang, Jean H" uniqKey="Chang J" first="Jean H." last="Chang">Jean H. Chang</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Chang, Stewart T" sort="Chang, Stewart T" uniqKey="Chang S" first="Stewart T." last="Chang">Stewart T. Chang</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Belisle, Sarah E" sort="Belisle, Sarah E" uniqKey="Belisle S" first="Sarah E." last="Belisle">Sarah E. Belisle</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Tumpey, Terrence M" sort="Tumpey, Terrence M" uniqKey="Tumpey T" first="Terrence M." last="Tumpey">Terrence M. Tumpey</name><affiliation wicri:level="2"><inist:fA14 i1="02"><s1>Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention</s1><s2>Atlanta, Georgia</s2><s3>USA</s3><sZ>2 aut.</sZ><sZ>7 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Katze, Michael G" sort="Katze, Michael G" uniqKey="Katze M" first="Michael G." last="Katze">Michael G. Katze</name><affiliation wicri:level="4"><inist:fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></inist:fA14><country>États-Unis</country><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author></analytic><series><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc><seriesStmt><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adaptation</term><term>Influenza A virus</term><term>Interferon</term><term>Macrophage</term><term>Virulence</term></keywords><keywords scheme="Pascal" xml:lang="fr"><term>Virus grippal A</term><term>Macrophage</term><term>Interféron</term><term>Virulence</term><term>Adaptation</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">While pandemic 2009 H1N1 influenza A viruses were responsible for numerous severe infections in humans, these viruses do not typically cause corresponding severe disease in mammalian models. However, the generation of a virulent 2009 H1N1 virus following serial lung passage in mice has allowed for the modeling of human lung pathology in this species. Genetic determinants of mouse-adapted 2009 H1N1 viral pathogenicity have been identified, but the molecular and signaling characteristics of the host response following infection with this adapted virus have not been described. Here we compared the gene expression response following infection of mice with A/CA/04/2009 (CA/04) or the virulent mouse-adapted strain (MA-CA/04). Microarray analysis revealed that increased pathogenicity of MA-CA/04 was associated with the following: (i) an early and sustained inflammatory and interferon response that could be driven in part by interferon regulatory factors (IRFs) and increased NF-<sub>K</sub>B activation, as well as inhibition of the negative regulator TRIM24, (ii) early and persistent infiltration of immune cells, including inflammatory macrophages, and (iii) the absence of activation of lipid metabolism later in infection, which may be mediated by inhibition of nuclear receptors, including PPARG and HNF1A and -4A, with proinflammatory consequences. Further investigation of these signatures in the host response to other H1N1 viruses of various pathogenicities confirmed their general relevance for virulence of influenza virus and suggested that lung response to MA-CA/04 virus was similar to that following infection with lethal H1N1 r1918 influenza virus. This study links differential activation of IRFs, nuclear receptors, and macrophage infiltration with influenza virulence in vivo.</div></front></TEI><inist><standard h6="B"><pA><fA01 i1="01" i2="1"><s0>0022-538X</s0></fA01><fA03 i2="1"><s0>J. virol.</s0></fA03><fA05><s2>86</s2></fA05><fA06><s2>13</s2></fA06><fA08 i1="01" i2="1" l="ENG"><s1>Implication of Inflammatory Macrophages, Nuclear Receptors, and Interferon Regulatory Factors in Increased Virulence of Pandemic 2009 H1N1 Influenza A Virus after Host Adaptation</s1></fA08><fA11 i1="01" i2="1"><s1>JOSSET (Laurence)</s1></fA11><fA11 i1="02" i2="1"><s1>BELSER (Jessica A.)</s1></fA11><fA11 i1="03" i2="1"><s1>PANTIN-JACKWOOD (Mary J.)</s1></fA11><fA11 i1="04" i2="1"><s1>CHANG (Jean H.)</s1></fA11><fA11 i1="05" i2="1"><s1>CHANG (Stewart T.)</s1></fA11><fA11 i1="06" i2="1"><s1>BELISLE (Sarah E.)</s1></fA11><fA11 i1="07" i2="1"><s1>TUMPEY (Terrence M.)</s1></fA11><fA11 i1="08" i2="1"><s1>KATZE (Michael G.)</s1></fA11><fA14 i1="01"><s1>Department of Microbiology, School of Medicine, University of Washington</s1><s2>Seattle, Washington</s2><s3>USA</s3><sZ>1 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>8 aut.</sZ></fA14><fA14 i1="02"><s1>Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention</s1><s2>Atlanta, Georgia</s2><s3>USA</s3><sZ>2 aut.</sZ><sZ>7 aut.</sZ></fA14><fA14 i1="03"><s1>Southeast Poultry Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture</s1><s2>Athens, GA</s2><s3>USA</s3><sZ>3 aut.</sZ></fA14><fA20><s1>7192-7206</s1></fA20><fA21><s1>2012</s1></fA21><fA23 i1="01"><s0>ENG</s0></fA23><fA43 i1="01"><s1>INIST</s1><s2>13592</s2><s5>354000507992960170</s5></fA43><fA44><s0>0000</s0><s1>© 2012 INIST-CNRS. All rights reserved.</s1></fA44><fA45><s0>57 ref.</s0></fA45><fA47 i1="01" i2="1"><s0>12-0269098</s0></fA47><fA60><s1>P</s1></fA60><fA61><s0>A</s0></fA61><fA64 i1="01" i2="1"><s0>Journal of virology</s0></fA64><fA66 i1="01"><s0>USA</s0></fA66><fC01 i1="01" l="ENG"><s0>While pandemic 2009 H1N1 influenza A viruses were responsible for numerous severe infections in humans, these viruses do not typically cause corresponding severe disease in mammalian models. However, the generation of a virulent 2009 H1N1 virus following serial lung passage in mice has allowed for the modeling of human lung pathology in this species. Genetic determinants of mouse-adapted 2009 H1N1 viral pathogenicity have been identified, but the molecular and signaling characteristics of the host response following infection with this adapted virus have not been described. Here we compared the gene expression response following infection of mice with A/CA/04/2009 (CA/04) or the virulent mouse-adapted strain (MA-CA/04). Microarray analysis revealed that increased pathogenicity of MA-CA/04 was associated with the following: (i) an early and sustained inflammatory and interferon response that could be driven in part by interferon regulatory factors (IRFs) and increased NF-<sub>K</sub>B activation, as well as inhibition of the negative regulator TRIM24, (ii) early and persistent infiltration of immune cells, including inflammatory macrophages, and (iii) the absence of activation of lipid metabolism later in infection, which may be mediated by inhibition of nuclear receptors, including PPARG and HNF1A and -4A, with proinflammatory consequences. Further investigation of these signatures in the host response to other H1N1 viruses of various pathogenicities confirmed their general relevance for virulence of influenza virus and suggested that lung response to MA-CA/04 virus was similar to that following infection with lethal H1N1 r1918 influenza virus. This study links differential activation of IRFs, nuclear receptors, and macrophage infiltration with influenza virulence in vivo.</s0></fC01><fC02 i1="01" i2="X"><s0>002A05C10</s0></fC02><fC03 i1="01" i2="X" l="FRE"><s0>Virus grippal A</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="01" i2="X" l="ENG"><s0>Influenza A virus</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="01" i2="X" l="SPA"><s0>Influenza A virus</s0><s2>NW</s2><s5>01</s5></fC03><fC03 i1="02" i2="X" l="FRE"><s0>Macrophage</s0><s5>05</s5></fC03><fC03 i1="02" i2="X" l="ENG"><s0>Macrophage</s0><s5>05</s5></fC03><fC03 i1="02" i2="X" l="SPA"><s0>Macrófago</s0><s5>05</s5></fC03><fC03 i1="03" i2="X" l="FRE"><s0>Interféron</s0><s2>NK</s2><s2>FR</s2><s5>06</s5></fC03><fC03 i1="03" i2="X" l="ENG"><s0>Interferon</s0><s2>NK</s2><s2>FR</s2><s5>06</s5></fC03><fC03 i1="03" i2="X" l="SPA"><s0>Interferón</s0><s2>NK</s2><s2>FR</s2><s5>06</s5></fC03><fC03 i1="04" i2="X" l="FRE"><s0>Virulence</s0><s5>07</s5></fC03><fC03 i1="04" i2="X" l="ENG"><s0>Virulence</s0><s5>07</s5></fC03><fC03 i1="04" i2="X" l="SPA"><s0>Virulencia</s0><s5>07</s5></fC03><fC03 i1="05" i2="X" l="FRE"><s0>Adaptation</s0><s5>08</s5></fC03><fC03 i1="05" i2="X" l="ENG"><s0>Adaptation</s0><s5>08</s5></fC03><fC03 i1="05" i2="X" l="SPA"><s0>Adaptación</s0><s5>08</s5></fC03><fC07 i1="01" i2="X" l="FRE"><s0>Influenzavirus A</s0><s2>NW</s2></fC07><fC07 i1="01" i2="X" l="ENG"><s0>Influenzavirus A</s0><s2>NW</s2></fC07><fC07 i1="01" i2="X" l="SPA"><s0>Influenzavirus A</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="FRE"><s0>Orthomyxoviridae</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="ENG"><s0>Orthomyxoviridae</s0><s2>NW</s2></fC07><fC07 i1="02" i2="X" l="SPA"><s0>Orthomyxoviridae</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="FRE"><s0>Virus</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="ENG"><s0>Virus</s0><s2>NW</s2></fC07><fC07 i1="03" i2="X" l="SPA"><s0>Virus</s0><s2>NW</s2></fC07><fN21><s1>205</s1></fN21><fN44 i1="01"><s1>OTO</s1></fN44><fN82><s1>OTO</s1></fN82></pA></standard></inist><affiliations><list><country><li>États-Unis</li></country><region><li>Géorgie (États-Unis)</li><li>Washington (État)</li></region><settlement><li>Seattle</li></settlement><orgName><li>Université de Washington</li></orgName></list><tree><country name="États-Unis"><region name="Washington (État)"><name sortKey="Josset, Laurence" sort="Josset, Laurence" uniqKey="Josset L" first="Laurence" last="Josset">Laurence Josset</name></region><name sortKey="Belisle, Sarah E" sort="Belisle, Sarah E" uniqKey="Belisle S" first="Sarah E." last="Belisle">Sarah E. Belisle</name><name sortKey="Belser, Jessica A" sort="Belser, Jessica A" uniqKey="Belser J" first="Jessica A." last="Belser">Jessica A. Belser</name><name sortKey="Chang, Jean H" sort="Chang, Jean H" uniqKey="Chang J" first="Jean H." last="Chang">Jean H. Chang</name><name sortKey="Chang, Stewart T" sort="Chang, Stewart T" uniqKey="Chang S" first="Stewart T." last="Chang">Stewart T. Chang</name><name sortKey="Katze, Michael G" sort="Katze, Michael G" uniqKey="Katze M" first="Michael G." last="Katze">Michael G. Katze</name><name sortKey="Pantin Jackwood, Mary J" sort="Pantin Jackwood, Mary J" uniqKey="Pantin Jackwood M" first="Mary J." last="Pantin-Jackwood">Mary J. Pantin-Jackwood</name><name sortKey="Tumpey, Terrence M" sort="Tumpey, Terrence M" uniqKey="Tumpey T" first="Terrence M." last="Tumpey">Terrence M. Tumpey</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|texte= Implication of Inflammatory Macrophages, Nuclear Receptors, and Interferon Regulatory Factors in Increased Virulence of Pandemic 2009 H1N1 Influenza A Virus after Host Adaptation
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