The Low-pH Stability Discovered in Neuraminidase of 1918 Pandemic Influenza A Virus Enhances Virus Replication
Identifieur interne : 000B17 ( Pmc/Curation ); précédent : 000B16; suivant : 000B18The Low-pH Stability Discovered in Neuraminidase of 1918 Pandemic Influenza A Virus Enhances Virus Replication
Auteurs : Tadanobu Takahashi [Japon] ; Yuuki Kurebayashi [Japon] ; Kumiko Ikeya [Japon] ; Takashi Mizuno [Japon] ; Keijo Fukushima [Japon] ; Hiroko Kawamoto [Japon] ; Yoshihiro Kawaoka [Japon, États-Unis] ; Yasuo Suzuki [Japon] ; Takashi Suzuki [Japon]Source :
- PLoS ONE [ 1932-6203 ] ; 2010.
Abstract
The “Spanish” pandemic influenza A virus, which killed more than 20 million worldwide in 1918-19, is one of the serious pathogens in recorded history. Characterization of the 1918 pandemic virus reconstructed by reverse genetics showed that PB1, hemagglutinin (HA), and neuraminidase (NA) genes contributed to the viral replication and virulence of the 1918 pandemic influenza virus. However, the function of the NA gene has remained unknown. Here we show that the avian-like low-pH stability of sialidase activity discovered in the 1918 pandemic virus NA contributes to the viral replication efficiency. We found that deletion of Thr at position 435 or deletion of Gly at position 455 in the 1918 pandemic virus NA was related to the low-pH stability of the sialidase activity in the 1918 pandemic virus NA by comparison with the sequences of other human N1 NAs and sialidase activity of chimeric constructs. Both amino acids were located in or near the amino acid resides that were important for stabilization of the native tetramer structure in a low-pH condition like the N2 NAs of pandemic viruses that emerged in 1957 and 1968. Two reverse-genetic viruses were generated from a genetic background of A/WSN/33 (H1N1) that included low-pH-unstable N1 NA from A/USSR/92/77 (H1N1) and its counterpart N1 NA in which sialidase activity was converted to a low-pH-stable property by a deletion and substitutions of two amino acid residues at position 435 and 455 related to the low-pH stability of the sialidase activity in 1918 NA. The mutant virus that included “Spanish Flu”-like low-pH-stable NA showed remarkable replication in comparison with the mutant virus that included low-pH-unstable N1 NA. Our results suggest that the avian-like low-pH stability of sialidase activity in the 1918 pandemic virus NA contributes to the viral replication efficiency.
Url:
DOI: 10.1371/journal.pone.0015556
PubMed: 21151571
PubMed Central: 3000343
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Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation></author><author><name sortKey="Kurebayashi, Yuuki" sort="Kurebayashi, Yuuki" uniqKey="Kurebayashi Y" first="Yuuki" last="Kurebayashi">Yuuki Kurebayashi</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation></author><author><name sortKey="Ikeya, Kumiko" sort="Ikeya, Kumiko" uniqKey="Ikeya K" first="Kumiko" last="Ikeya">Kumiko Ikeya</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation></author><author><name sortKey="Mizuno, Takashi" sort="Mizuno, Takashi" uniqKey="Mizuno T" first="Takashi" last="Mizuno">Takashi Mizuno</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation></author><author><name sortKey="Fukushima, Keijo" sort="Fukushima, Keijo" uniqKey="Fukushima K" first="Keijo" last="Fukushima">Keijo Fukushima</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation></author><author><name sortKey="Kawamoto, Hiroko" sort="Kawamoto, Hiroko" uniqKey="Kawamoto H" first="Hiroko" last="Kawamoto">Hiroko Kawamoto</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation></author><author><name sortKey="Kawaoka, Yoshihiro" sort="Kawaoka, Yoshihiro" uniqKey="Kawaoka Y" first="Yoshihiro" last="Kawaoka">Yoshihiro Kawaoka</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin</wicri:regionArea></affiliation></author><author><name sortKey="Suzuki, Yasuo" sort="Suzuki, Yasuo" uniqKey="Suzuki Y" first="Yasuo" last="Suzuki">Yasuo Suzuki</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>Department of Biomedical Sciences, College of Life and Health Sciences, Chubu University, Kasugai-shi, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biomedical Sciences, College of Life and Health Sciences, Chubu University, Kasugai-shi</wicri:regionArea></affiliation></author><author><name sortKey="Suzuki, Takashi" sort="Suzuki, Takashi" uniqKey="Suzuki T" first="Takashi" last="Suzuki">Takashi Suzuki</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>CREST, Japan Science and Technology Agency, Saitama</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</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>The “Spanish” pandemic influenza A virus, which killed more than 20 million worldwide in 1918-19, is one of the serious pathogens in recorded history. Characterization of the 1918 pandemic virus reconstructed by reverse genetics showed that PB1, hemagglutinin (HA), and neuraminidase (NA) genes contributed to the viral replication and virulence of the 1918 pandemic influenza virus. However, the function of the NA gene has remained unknown. Here we show that the avian-like low-pH stability of sialidase activity discovered in the 1918 pandemic virus NA contributes to the viral replication efficiency. We found that deletion of Thr at position 435 or deletion of Gly at position 455 in the 1918 pandemic virus NA was related to the low-pH stability of the sialidase activity in the 1918 pandemic virus NA by comparison with the sequences of other human N1 NAs and sialidase activity of chimeric constructs. Both amino acids were located in or near the amino acid resides that were important for stabilization of the native tetramer structure in a low-pH condition like the N2 NAs of pandemic viruses that emerged in 1957 and 1968. Two reverse-genetic viruses were generated from a genetic background of A/WSN/33 (H1N1) that included low-pH-unstable N1 NA from A/USSR/92/77 (H1N1) and its counterpart N1 NA in which sialidase activity was converted to a low-pH-stable property by a deletion and substitutions of two amino acid residues at position 435 and 455 related to the low-pH stability of the sialidase activity in 1918 NA. The mutant virus that included “Spanish Flu”-like low-pH-stable NA showed remarkable replication in comparison with the mutant virus that included low-pH-unstable N1 NA. Our results suggest that the avian-like low-pH stability of sialidase activity in the 1918 pandemic virus NA contributes to the viral replication efficiency.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Pappas, C" uniqKey="Pappas C">C Pappas</name></author><author><name sortKey="Aguilar, Pv" uniqKey="Aguilar P">PV Aguilar</name></author><author><name sortKey="Basler, Cf" uniqKey="Basler C">CF Basler</name></author><author><name sortKey="Solorzano, A" uniqKey="Solorzano A">A Solorzano</name></author><author><name sortKey="Zeng, H" uniqKey="Zeng H">H Zeng</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Conenello, Gm" uniqKey="Conenello G">GM Conenello</name></author><author><name sortKey="Zamarin, D" uniqKey="Zamarin D">D Zamarin</name></author><author><name sortKey="Perrone, La" uniqKey="Perrone L">LA Perrone</name></author><author><name sortKey="Tumpey, T" uniqKey="Tumpey T">T 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">21151571</article-id><article-id pub-id-type="pmc">3000343</article-id><article-id pub-id-type="publisher-id">PONE-D-10-00536</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0015556</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Protein Structure</subject></subj-group></subj-group><subj-group><subject>Enzymes</subject><subject>Glycobiology</subject></subj-group></subj-group><subj-group><subject>Computational Biology</subject><subj-group><subject>Macromolecular Structure Analysis</subject><subj-group><subject>Protein Structure</subject></subj-group></subj-group></subj-group><subj-group><subject>Genetics</subject><subj-group><subject>Genetic Mutation</subject><subject>Molecular Genetics</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Evolution</subject><subject>Viral Replication</subject><subject>Viral Structure</subject><subject>Virulence Factors and Mechanisms</subject></subj-group></subj-group><subj-group><subject>Host-Pathogen Interaction</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>The Low-pH Stability Discovered in Neuraminidase of 1918 Pandemic Influenza A Virus Enhances Virus Replication</article-title><alt-title alt-title-type="running-head">The Low-pH Stability of 1918 Pandemic Virus N1NA</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Takahashi</surname><given-names>Tadanobu</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kurebayashi</surname><given-names>Yuuki</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ikeya</surname><given-names>Kumiko</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mizuno</surname><given-names>Takashi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Fukushima</surname><given-names>Keijo</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kawamoto</surname><given-names>Hiroko</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kawaoka</surname><given-names>Yoshihiro</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Suzuki</surname><given-names>Yasuo</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Suzuki</surname><given-names>Takashi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Department of Biochemistry, University of Shizuoka, School of Pharmaceutical Sciences and Global COE Program for Innovation in Human Health Sciences, Shizuoka, Japan</addr-line></aff><aff id="aff2"><label>2</label><addr-line>CREST, Japan Science and Technology Agency, Saitama, Japan</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo, Japan</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin, United States of America</addr-line></aff><aff id="aff5"><label>5</label><addr-line>Department of Biomedical Sciences, College of Life and Health Sciences, Chubu University, Kasugai-shi, Japan</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Digard</surname><given-names>Paul</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">University of Cambridge, United Kingdom</aff><author-notes><corresp id="cor1">* E-mail: <email>Suzukit@u-shizuoka-ken.ac.jp</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: TT TS. Performed the experiments: TT YK KI TM KF HK. Analyzed the data: TT YK TS. Contributed reagents/materials/analysis tools: YK YS. Wrote the paper: TT TS.</p></fn></author-notes><pub-date pub-type="collection"><year>2010</year></pub-date><pub-date pub-type="epub"><day>9</day><month>12</month><year>2010</year></pub-date><volume>5</volume><issue>12</issue><elocation-id>e15556</elocation-id><history><date date-type="received"><day>9</day><month>8</month><year>2010</year></date><date date-type="accepted"><day>12</day><month>11</month><year>2010</year></date></history><permissions><copyright-statement>Takahashi et al.</copyright-statement><copyright-year>2010</copyright-year><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><p>The “Spanish” pandemic influenza A virus, which killed more than 20 million worldwide in 1918-19, is one of the serious pathogens in recorded history. Characterization of the 1918 pandemic virus reconstructed by reverse genetics showed that PB1, hemagglutinin (HA), and neuraminidase (NA) genes contributed to the viral replication and virulence of the 1918 pandemic influenza virus. However, the function of the NA gene has remained unknown. Here we show that the avian-like low-pH stability of sialidase activity discovered in the 1918 pandemic virus NA contributes to the viral replication efficiency. We found that deletion of Thr at position 435 or deletion of Gly at position 455 in the 1918 pandemic virus NA was related to the low-pH stability of the sialidase activity in the 1918 pandemic virus NA by comparison with the sequences of other human N1 NAs and sialidase activity of chimeric constructs. Both amino acids were located in or near the amino acid resides that were important for stabilization of the native tetramer structure in a low-pH condition like the N2 NAs of pandemic viruses that emerged in 1957 and 1968. Two reverse-genetic viruses were generated from a genetic background of A/WSN/33 (H1N1) that included low-pH-unstable N1 NA from A/USSR/92/77 (H1N1) and its counterpart N1 NA in which sialidase activity was converted to a low-pH-stable property by a deletion and substitutions of two amino acid residues at position 435 and 455 related to the low-pH stability of the sialidase activity in 1918 NA. The mutant virus that included “Spanish Flu”-like low-pH-stable NA showed remarkable replication in comparison with the mutant virus that included low-pH-unstable N1 NA. Our results suggest that the avian-like low-pH stability of sialidase activity in the 1918 pandemic virus NA contributes to the viral replication efficiency.</p></abstract><counts><page-count count="7"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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