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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Integrated Clinical, Pathologic, Virologic, and Transcriptomic Analysis of H5N1 Influenza Virus-Induced Viral Pneumonia in the Rhesus Macaque</title>
<author><name sortKey="Shinya, Kyoko" sort="Shinya, Kyoko" uniqKey="Shinya K" first="Kyoko" last="Shinya">Kyoko Shinya</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gao, Yuwei" sort="Gao, Yuwei" uniqKey="Gao Y" first="Yuwei" last="Gao">Yuwei Gao</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cilloniz, Cristian" sort="Cilloniz, Cristian" uniqKey="Cilloniz C" first="Cristian" last="Cilloniz">Cristian Cilloniz</name>
<affiliation><nlm:aff id="aff3">Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Suzuki, Yasuhiro" sort="Suzuki, Yasuhiro" uniqKey="Suzuki Y" first="Yasuhiro" last="Suzuki">Yasuhiro Suzuki</name>
<affiliation><nlm:aff id="aff4">Department of Complex Systems Science, Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fujie, Masahiro" sort="Fujie, Masahiro" uniqKey="Fujie M" first="Masahiro" last="Fujie">Masahiro Fujie</name>
<affiliation><nlm:aff id="aff4">Department of Complex Systems Science, Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Guohua" sort="Deng, Guohua" uniqKey="Deng G" first="Guohua" last="Deng">Guohua Deng</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhu, Qiyun" sort="Zhu, Qiyun" uniqKey="Zhu Q" first="Qiyun" last="Zhu">Qiyun Zhu</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fan, Shufang" sort="Fan, Shufang" uniqKey="Fan S" first="Shufang" last="Fan">Shufang Fan</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Makino, Akiko" sort="Makino, Akiko" uniqKey="Makino A" first="Akiko" last="Makino">Akiko Makino</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Muramoto, Yukiko" sort="Muramoto, Yukiko" uniqKey="Muramoto Y" first="Yukiko" last="Muramoto">Yukiko Muramoto</name>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fukuyama, Satoshi" sort="Fukuyama, Satoshi" uniqKey="Fukuyama S" first="Satoshi" last="Fukuyama">Satoshi Fukuyama</name>
<affiliation><nlm:aff id="aff6">ERATO Infection-Induced Host Responses Project, Japan Science and Technology Agency, Saitama, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tamura, Daisuke" sort="Tamura, Daisuke" uniqKey="Tamura D" first="Daisuke" last="Tamura">Daisuke Tamura</name>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Noda, Takeshi" sort="Noda, Takeshi" uniqKey="Noda T" first="Takeshi" last="Noda">Takeshi Noda</name>
<affiliation><nlm:aff id="aff7">International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Eisfeld, Amie J" sort="Eisfeld, Amie J" uniqKey="Eisfeld A" first="Amie J." last="Eisfeld">Amie J. Eisfeld</name>
<affiliation><nlm:aff id="aff8">Influenza Research Institute, Department of Pathological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA</nlm:aff>
</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><nlm:aff id="aff3">Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Chen, Hualan" sort="Chen, Hualan" uniqKey="Chen H" first="Hualan" last="Chen">Hualan Chen</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kawaoka, Yoshihiro" sort="Kawaoka, Yoshihiro" uniqKey="Kawaoka Y" first="Yoshihiro" last="Kawaoka">Yoshihiro Kawaoka</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff6">ERATO Infection-Induced Host Responses Project, Japan Science and Technology Agency, Saitama, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff7">International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff8">Influenza Research Institute, Department of Pathological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">22491448</idno>
<idno type="pmc">3372212</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3372212</idno>
<idno type="RBID">PMC:3372212</idno>
<idno type="doi">10.1128/JVI.00365-12</idno>
<date when="2012">2012</date>
<idno type="wicri:Area/Pmc/Corpus">000648</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000648</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Integrated Clinical, Pathologic, Virologic, and Transcriptomic Analysis of H5N1 Influenza Virus-Induced Viral Pneumonia in the Rhesus Macaque</title>
<author><name sortKey="Shinya, Kyoko" sort="Shinya, Kyoko" uniqKey="Shinya K" first="Kyoko" last="Shinya">Kyoko Shinya</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gao, Yuwei" sort="Gao, Yuwei" uniqKey="Gao Y" first="Yuwei" last="Gao">Yuwei Gao</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cilloniz, Cristian" sort="Cilloniz, Cristian" uniqKey="Cilloniz C" first="Cristian" last="Cilloniz">Cristian Cilloniz</name>
<affiliation><nlm:aff id="aff3">Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Suzuki, Yasuhiro" sort="Suzuki, Yasuhiro" uniqKey="Suzuki Y" first="Yasuhiro" last="Suzuki">Yasuhiro Suzuki</name>
<affiliation><nlm:aff id="aff4">Department of Complex Systems Science, Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fujie, Masahiro" sort="Fujie, Masahiro" uniqKey="Fujie M" first="Masahiro" last="Fujie">Masahiro Fujie</name>
<affiliation><nlm:aff id="aff4">Department of Complex Systems Science, Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Guohua" sort="Deng, Guohua" uniqKey="Deng G" first="Guohua" last="Deng">Guohua Deng</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhu, Qiyun" sort="Zhu, Qiyun" uniqKey="Zhu Q" first="Qiyun" last="Zhu">Qiyun Zhu</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fan, Shufang" sort="Fan, Shufang" uniqKey="Fan S" first="Shufang" last="Fan">Shufang Fan</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Makino, Akiko" sort="Makino, Akiko" uniqKey="Makino A" first="Akiko" last="Makino">Akiko Makino</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Muramoto, Yukiko" sort="Muramoto, Yukiko" uniqKey="Muramoto Y" first="Yukiko" last="Muramoto">Yukiko Muramoto</name>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Fukuyama, Satoshi" sort="Fukuyama, Satoshi" uniqKey="Fukuyama S" first="Satoshi" last="Fukuyama">Satoshi Fukuyama</name>
<affiliation><nlm:aff id="aff6">ERATO Infection-Induced Host Responses Project, Japan Science and Technology Agency, Saitama, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tamura, Daisuke" sort="Tamura, Daisuke" uniqKey="Tamura D" first="Daisuke" last="Tamura">Daisuke Tamura</name>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Noda, Takeshi" sort="Noda, Takeshi" uniqKey="Noda T" first="Takeshi" last="Noda">Takeshi Noda</name>
<affiliation><nlm:aff id="aff7">International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Eisfeld, Amie J" sort="Eisfeld, Amie J" uniqKey="Eisfeld A" first="Amie J." last="Eisfeld">Amie J. Eisfeld</name>
<affiliation><nlm:aff id="aff8">Influenza Research Institute, Department of Pathological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA</nlm:aff>
</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><nlm:aff id="aff3">Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Chen, Hualan" sort="Chen, Hualan" uniqKey="Chen H" first="Hualan" last="Chen">Hualan Chen</name>
<affiliation><nlm:aff id="aff2">Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kawaoka, Yoshihiro" sort="Kawaoka, Yoshihiro" uniqKey="Kawaoka Y" first="Yoshihiro" last="Kawaoka">Yoshihiro Kawaoka</name>
<affiliation><nlm:aff id="aff1">Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff5">Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff6">ERATO Infection-Induced Host Responses Project, Japan Science and Technology Agency, Saitama, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff7">International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff8">Influenza Research Institute, Department of Pathological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
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<profileDesc><textClass></textClass>
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<front><div type="abstract" xml:lang="en"><p>Viral pneumonia has been frequently reported during early stages of influenza virus pandemics and in many human cases of highly pathogenic avian influenza (HPAI) H5N1 virus infection. To better understand the pathogenesis of this disease, we produced nonlethal viral pneumonia in rhesus macaques by using an HPAI H5N1 virus (A/Anhui/2/2005; referred to as Anhui/2). Infected macaques were monitored for 14 days, and tissue samples were collected at 6 time points for virologic, histopathologic, and transcriptomic analyses. Anhui/2 efficiently replicated in the lung from 12 h to 3 days postinfection (p.i.) and caused temporal but severe pneumonia that began to resolve by day 14. Lung transcriptional changes were first observed at 6 h, and increased expression of vascular permeability regulators and neutrophil chemoattractants correlated with increased serum leakage and neutrophil infiltration <italic>in situ</italic>
. Additional inflammatory, antiviral, and apoptotic genes were upregulated from 12 h, concurrent with viral antigen detection and increasing immune cell populations. A shift toward upregulation of acquired immunity was apparent after day 6. Expression levels of established immune cell molecular markers revealed remarkable similarity with pathological findings, indicating early and robust neutrophil infiltration, a slight delay in macrophage accumulation, and abundant late populations of T lymphocytes. We also characterized the putative mechanisms regulating a unique, pneumonia-associated biphasic fever pattern. Thus, this study is the first to use a comprehensive and integrative approach to delineate specific molecular mechanisms regulating influenza virus-induced pneumonia in nonhuman primates, an important first step toward better management of human influenza virus disease.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group><journal-title>Journal of Virology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22491448</article-id>
<article-id pub-id-type="pmc">3372212</article-id>
<article-id pub-id-type="publisher-id">00365-12</article-id>
<article-id pub-id-type="doi">10.1128/JVI.00365-12</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Pathogenesis and Immunity</subject>
</subj-group>
</article-categories>
<title-group><article-title>Integrated Clinical, Pathologic, Virologic, and Transcriptomic Analysis of H5N1 Influenza Virus-Induced Viral Pneumonia in the Rhesus Macaque</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Shinya</surname>
<given-names>Kyoko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gao</surname>
<given-names>Yuwei</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cilloniz</surname>
<given-names>Cristian</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Suzuki</surname>
<given-names>Yasuhiro</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fujie</surname>
<given-names>Masahiro</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Deng</surname>
<given-names>Guohua</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhu</surname>
<given-names>Qiyun</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fan</surname>
<given-names>Shufang</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Makino</surname>
<given-names>Akiko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Muramoto</surname>
<given-names>Yukiko</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fukuyama</surname>
<given-names>Satoshi</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tamura</surname>
<given-names>Daisuke</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Noda</surname>
<given-names>Takeshi</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Eisfeld</surname>
<given-names>Amie J.</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Katze</surname>
<given-names>Michael G.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Chen</surname>
<given-names>Hualan</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Kawaoka</surname>
<given-names>Yoshihiro</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
Division of Zoonosis, Department of Microbiology and Infectious Disease, Graduate School of Medicine, Kobe University, Kusunoki-cho, Chuo-ku, Kobe, Hyogo, Japan</aff>
<aff id="aff2"><label>b</label>
Animal Influenza Laboratory of the Ministry of Agriculture and State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, People's Republic of China</aff>
<aff id="aff3"><label>c</label>
Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA</aff>
<aff id="aff4"><label>d</label>
Department of Complex Systems Science, Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan</aff>
<aff id="aff5"><label>e</label>
Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</aff>
<aff id="aff6"><label>f</label>
ERATO Infection-Induced Host Responses Project, Japan Science and Technology Agency, Saitama, Japan</aff>
<aff id="aff7"><label>g</label>
International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Shirokanedai, Minato-ku, Tokyo, Japan</aff>
<aff id="aff8"><label>h</label>
Influenza Research Institute, Department of Pathological Sciences, University of Wisconsin—Madison, Madison, Wisconsin, USA</aff>
</contrib-group>
<author-notes><corresp>Address correspondence to Yoshihiro Kawaoka, <email>kawaoka@ims.u-tokyo.ac.jp</email>
, or Hualan Chen, <email>hlchen1@yahoo.com</email>
.</corresp>
<fn fn-type="equal"><p>K.S., Y.G., and C.C. contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>6</month>
<year>2012</year>
</pub-date>
<volume>86</volume>
<issue>11</issue>
<fpage>6055</fpage>
<lpage>6066</lpage>
<history><date date-type="received"><day>27</day>
<month>2</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>19</day>
<month>3</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2012, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2012</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
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<abstract><p>Viral pneumonia has been frequently reported during early stages of influenza virus pandemics and in many human cases of highly pathogenic avian influenza (HPAI) H5N1 virus infection. To better understand the pathogenesis of this disease, we produced nonlethal viral pneumonia in rhesus macaques by using an HPAI H5N1 virus (A/Anhui/2/2005; referred to as Anhui/2). Infected macaques were monitored for 14 days, and tissue samples were collected at 6 time points for virologic, histopathologic, and transcriptomic analyses. Anhui/2 efficiently replicated in the lung from 12 h to 3 days postinfection (p.i.) and caused temporal but severe pneumonia that began to resolve by day 14. Lung transcriptional changes were first observed at 6 h, and increased expression of vascular permeability regulators and neutrophil chemoattractants correlated with increased serum leakage and neutrophil infiltration <italic>in situ</italic>
. Additional inflammatory, antiviral, and apoptotic genes were upregulated from 12 h, concurrent with viral antigen detection and increasing immune cell populations. A shift toward upregulation of acquired immunity was apparent after day 6. Expression levels of established immune cell molecular markers revealed remarkable similarity with pathological findings, indicating early and robust neutrophil infiltration, a slight delay in macrophage accumulation, and abundant late populations of T lymphocytes. We also characterized the putative mechanisms regulating a unique, pneumonia-associated biphasic fever pattern. Thus, this study is the first to use a comprehensive and integrative approach to delineate specific molecular mechanisms regulating influenza virus-induced pneumonia in nonhuman primates, an important first step toward better management of human influenza virus disease.</p>
</abstract>
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