Prevalence, genetics, and transmissibility in ferrets of Eurasian avian-like H1N1 swine influenza viruses
Identifieur interne : 000071 ( Pmc/Curation ); précédent : 000070; suivant : 000072Prevalence, genetics, and transmissibility in ferrets of Eurasian avian-like H1N1 swine influenza viruses
Auteurs : Huanliang Yang [République populaire de Chine] ; Yan Chen [République populaire de Chine] ; Chuanling Qiao [République populaire de Chine] ; Xijun He [République populaire de Chine] ; Hong Zhou [République populaire de Chine] ; Yu Sun [République populaire de Chine] ; Hang Yin [République populaire de Chine] ; Shasha Meng [République populaire de Chine] ; Liping Liu [République populaire de Chine] ; Qianyi Zhang [République populaire de Chine] ; Huihui Kong [République populaire de Chine] ; Chunyang Gu [République populaire de Chine] ; Chengjun Li [République populaire de Chine] ; Zhigao Bu [République populaire de Chine] ; Yoshihiro Kawaoka [Japon] ; Hualan Chen [République populaire de Chine]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2015.
Abstract
Animal influenza viruses continue to challenge human public health; surveillance of these viruses and evaluation of their pandemic potential are important for future influenza pandemic preparedness. Pigs are intermediate hosts for novel influenza generation and transfer to humans. Two lineages of H1N1 swine influenza viruses (SIVs), classical H1N1 SIVs and Eurasian avian-like H1N1 (EAH1N1) SIVs, have been circulating in pigs since 1918 and 1979, respectively. The classical H1N1 SIVs emerged in humans as a reassortant and caused the 2009 H1N1 influenza pandemic. Here, we found that, after long-term evolution in pigs, the EAH1N1 SIVs have obtained the traits to cause a human influenza pandemic.
Url:
DOI: 10.1073/pnas.1522643113
PubMed: 26711995
PubMed Central: 4720320
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<author><name sortKey="Yin, Hang" sort="Yin, Hang" uniqKey="Yin H" first="Hang" last="Yin">Hang Yin</name>
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<author><name sortKey="Meng, Shasha" sort="Meng, Shasha" uniqKey="Meng S" first="Shasha" last="Meng">Shasha Meng</name>
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<author><name sortKey="Liu, Liping" sort="Liu, Liping" uniqKey="Liu L" first="Liping" last="Liu">Liping Liu</name>
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<author><name sortKey="Zhang, Qianyi" sort="Zhang, Qianyi" uniqKey="Zhang Q" first="Qianyi" last="Zhang">Qianyi Zhang</name>
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<author><name sortKey="Kong, Huihui" sort="Kong, Huihui" uniqKey="Kong H" first="Huihui" last="Kong">Huihui Kong</name>
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<author><name sortKey="Gu, Chunyang" sort="Gu, Chunyang" uniqKey="Gu C" first="Chunyang" last="Gu">Chunyang Gu</name>
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<author><name sortKey="Li, Chengjun" sort="Li, Chengjun" uniqKey="Li C" first="Chengjun" last="Li">Chengjun Li</name>
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<author><name sortKey="Kawaoka, Yoshihiro" sort="Kawaoka, Yoshihiro" uniqKey="Kawaoka Y" first="Yoshihiro" last="Kawaoka">Yoshihiro Kawaoka</name>
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<author><name sortKey="Chen, Hualan" sort="Chen, Hualan" uniqKey="Chen H" first="Hualan" last="Chen">Hualan Chen</name>
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<author><name sortKey="Sun, Yu" sort="Sun, Yu" uniqKey="Sun Y" first="Yu" last="Sun">Yu Sun</name>
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<author><name sortKey="Yin, Hang" sort="Yin, Hang" uniqKey="Yin H" first="Hang" last="Yin">Hang Yin</name>
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<author><name sortKey="Meng, Shasha" sort="Meng, Shasha" uniqKey="Meng S" first="Shasha" last="Meng">Shasha Meng</name>
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, Harbin 150001,<country>People’s Republic of China</country>
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<author><name sortKey="Liu, Liping" sort="Liu, Liping" uniqKey="Liu L" first="Liping" last="Liu">Liping Liu</name>
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, Harbin 150001,<country>People’s Republic of China</country>
;</nlm:aff>
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<author><name sortKey="Zhang, Qianyi" sort="Zhang, Qianyi" uniqKey="Zhang Q" first="Qianyi" last="Zhang">Qianyi Zhang</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute,<institution>Chinese Academy of Agricultural Sciences</institution>
, Harbin 150001,<country>People’s Republic of China</country>
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<author><name sortKey="Kong, Huihui" sort="Kong, Huihui" uniqKey="Kong H" first="Huihui" last="Kong">Huihui Kong</name>
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, Harbin 150001,<country>People’s Republic of China</country>
;</nlm:aff>
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<author><name sortKey="Gu, Chunyang" sort="Gu, Chunyang" uniqKey="Gu C" first="Chunyang" last="Gu">Chunyang Gu</name>
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, Harbin 150001,<country>People’s Republic of China</country>
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<author><name sortKey="Li, Chengjun" sort="Li, Chengjun" uniqKey="Li C" first="Chengjun" last="Li">Chengjun Li</name>
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;</nlm:aff>
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</nlm:aff>
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;</nlm:aff>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>Animal influenza viruses continue to challenge human public health; surveillance of these viruses and evaluation of their pandemic potential are important for future influenza pandemic preparedness. Pigs are intermediate hosts for novel influenza generation and transfer to humans. Two lineages of H1N1 swine influenza viruses (SIVs), classical H1N1 SIVs and Eurasian avian-like H1N1 (EAH1N1) SIVs, have been circulating in pigs since 1918 and 1979, respectively. The classical H1N1 SIVs emerged in humans as a reassortant and caused the 2009 H1N1 influenza pandemic. Here, we found that, after long-term evolution in pigs, the EAH1N1 SIVs have obtained the traits to cause a human influenza pandemic.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
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<article-id pub-id-type="publisher-id">201522643</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1522643113</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Microbiology</subject>
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<title-group><article-title>Prevalence, genetics, and transmissibility in ferrets of Eurasian avian-like H1N1 swine influenza viruses</article-title>
<alt-title alt-title-type="short">Avian-like H1N1 swine influenza in China</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Huanliang</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Yan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Qiao</surname>
<given-names>Chuanling</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>He</surname>
<given-names>Xijun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Hong</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sun</surname>
<given-names>Yu</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yin</surname>
<given-names>Hang</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meng</surname>
<given-names>Shasha</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Liping</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Qianyi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kong</surname>
<given-names>Huihui</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gu</surname>
<given-names>Chunyang</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Chengjun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bu</surname>
<given-names>Zhigao</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kawaoka</surname>
<given-names>Yoshihiro</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Hualan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute,<institution>Chinese Academy of Agricultural Sciences</institution>
, Harbin 150001,<country>People’s Republic of China</country>
;</aff>
<aff id="aff2"><sup>b</sup>
<institution>The First Hospital of Harbin Medical University</institution>
, Harbin 150070,<country>China</country>
;</aff>
<aff id="aff3"><sup>c</sup>
Division of Virology, Department of Microbiology and Immunology, International Research Center for Infectious Diseases, Institute of Medical Science,<institution>University of Tokyo</institution>
, 4-6-1, Shirokanedai, Minato-ku, Tokyo 108-8639,<country>Japan</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>2</sup>
To whom correspondence may be addressed. Email: <email>kawaokay@svm.vetmed.wisc.edu</email>
or <email>chenhualan@caas.cn</email>
.</corresp>
<fn fn-type="edited-by"><p>Contributed by Yoshihiro Kawaoka, November 19, 2015 (sent for review September 2, 2015; reviewed by Ruben Donis and Hans-Dieter Klenk)</p>
</fn>
<fn fn-type="con"><p>Author contributions: H. Yang, Y.C., C.Q., Z.B., and H.C. designed research; H. Yang, Y.C., C.Q., X.H., H.Z., Y.S., H. Yin, S.M., L.L., Q.Z., H.K., and C.G. performed research; H. Yang, Y.C., C.Q., C.L., Z.B., Y.K., and H.C. analyzed data; and H. Yang, Z.B., Y.K., and H.C. wrote the paper.</p>
</fn>
<fn fn-type="con"><p>Reviewers: R.D., Center for Disease Control; and H.-D.K., Philipps-Universitat Marburg.</p>
</fn>
<fn fn-type="equal" id="fn1"><p><sup>1</sup>
H. Yang, Y.C., and C.Q. contributed equally to this work.</p>
</fn>
<fn fn-type="conflict"><p>Conflict of interest statement: Y.K. has received speaker’s honoraria from Toyama Chemical and Astellas Inc.; has received grant support from Chugai Pharmaceuticals, Daiichi Sankyo Pharmaceutical, Toyama Chemical, Tauns Laboratories, Inc., and Otsuka Pharmaceutical Co., Ltd; and is a founder of FluGen.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>12</day>
<month>1</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>28</day>
<month>12</month>
<year>2015</year>
</pub-date>
<volume>113</volume>
<issue>2</issue>
<fpage>392</fpage>
<lpage>397</lpage>
<permissions></permissions>
<self-uri xlink:title="pdf" xlink:href="pnas.201522643.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>Animal influenza viruses continue to challenge human public health; surveillance of these viruses and evaluation of their pandemic potential are important for future influenza pandemic preparedness. Pigs are intermediate hosts for novel influenza generation and transfer to humans. Two lineages of H1N1 swine influenza viruses (SIVs), classical H1N1 SIVs and Eurasian avian-like H1N1 (EAH1N1) SIVs, have been circulating in pigs since 1918 and 1979, respectively. The classical H1N1 SIVs emerged in humans as a reassortant and caused the 2009 H1N1 influenza pandemic. Here, we found that, after long-term evolution in pigs, the EAH1N1 SIVs have obtained the traits to cause a human influenza pandemic.</p>
</abstract>
<abstract><p>Pigs are important intermediate hosts for generating novel influenza viruses. The Eurasian avian-like H1N1 (EAH1N1) swine influenza viruses (SIVs) have circulated in pigs since 1979, and human cases associated with EAH1N1 SIVs have been reported in several countries. However, the biologic properties of EAH1N1 SIVs are largely unknown. Here, we performed extensive influenza surveillance in pigs in China and isolated 228 influenza viruses from 36,417 pigs. We found that 139 of the 228 strains from pigs in 10 provinces in China belong to the EAH1N1 lineage. These viruses formed five genotypes, with two distinct antigenic groups, represented by A/swine/Guangxi/18/2011 and A/swine/Guangdong/104/2013, both of which are antigenically and genetically distinct from the current human H1N1 viruses. Importantly, the EAH1N1 SIVs preferentially bound to human-type receptors, and 9 of the 10 tested viruses transmitted in ferrets by respiratory droplet. We found that 3.6% of children (≤10 y old), 0% of adults, and 13.4% of elderly adults (≥60 y old) had neutralization antibodies (titers ≥40 in children and ≥80 in adults) against the EAH1N1 A/swine/Guangxi/18/2011 virus, but none of them had such neutralization antibodies against the EAH1N1 A/swine/Guangdong/104/2013 virus. Our study shows the potential of EAH1N1 SIVs to transmit efficiently in humans and suggests that immediate action is needed to prevent the efficient transmission of EAH1N1 SIVs to humans.</p>
</abstract>
<kwd-group><kwd>swine influenza</kwd>
<kwd>H1N1</kwd>
<kwd>Eurasian lineage</kwd>
<kwd>evolution</kwd>
<kwd>pandemic potential</kwd>
</kwd-group>
<funding-group><award-group id="gs1"><funding-source id="sp1">National Natural Science Foundation of China (NSFC)<named-content content-type="funder-id">501100001809</named-content>
</funding-source>
<award-id rid="sp1">31302108</award-id>
<award-id rid="sp1">31521005</award-id>
</award-group>
<award-group id="gs2"><funding-source id="sp2">FAO</funding-source>
<award-id rid="sp2">CHN/2013/001/LOA</award-id>
</award-group>
<award-group id="gs3"><funding-source id="sp3">Japan Agency for Medical Research and Development, AMED</funding-source>
<award-id rid="sp3">Japan Initiative for Global Research Network on Infectious Diseases</award-id>
</award-group>
</funding-group>
<counts><page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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