Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets
Identifieur interne : 000769 ( Pmc/Curation ); précédent : 000768; suivant : 000770Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets
Auteurs : Tokiko Watanabe [États-Unis] ; Shinji Watanabe [États-Unis] ; Kyoko Shinya [Japon] ; Jin Hyun Kim [États-Unis] ; Masato Hatta [États-Unis] ; Yoshihiro Kawaoka [États-Unis, Japon]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2008.
Abstract
The 1918 influenza pandemic was the most devastating outbreak of infectious disease in human history, accounting for about 50 million deaths worldwide. In addition to a significant number of cases of secondary bacterial pneumonia, this highly pathogenic strain of influenza A virus caused fatal primary viral pneumonia. To identify the viral gene(s) chiefly responsible for the high virulence of the 1918 virus, we generated a series of reassortants between the 1918 virus and a contemporary human H1N1 virus (A/Kawasaki/173/2001; K173) using reverse genetics. We then assessed their virulence properties in ferrets, a model closely resembling humans in terms of sensitivity to influenza virus infection and pattern of spread after intranasal inoculation. Substitution of single genes from the 1918 virus in the genetic background of K173 virus did not markedly alter the pattern of infection. That is, the reassortants grew well in nasal turbinates, but only sporadically (if at all) in the trachea and lungs. One exception was the 1918PB1/K173 reassortant, which replicated efficiently in lung tissues as well as the upper respiratory tract. A reassortant virus expressing the 1918 viral RNA polymerase complex (PA, PB1, and PB2) and nucleoprotein showed virulence properties in the upper and lower respiratory tracts of ferrets that closely resembled those of wild-type 1918 virus. Our findings strongly implicate the viral RNA polymerase complex as a major determinant of the pathogenicity of the 1918 pandemic virus. This new insight may aid in identifying virulence factors in future pandemic viruses that could be targeted with antiviral compounds.
Url:
DOI: 10.1073/pnas.0806959106
PubMed: 19114663
PubMed Central: 2626747
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Yoshihiro Kawaoka<affiliation><nlm:aff wicri:cut=", and" id="aff3">Division of Virology, Department of Microbiology and Immunology</nlm:aff>
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<front><div type="abstract" xml:lang="en"><p>The 1918 influenza pandemic was the most devastating outbreak of infectious disease in human history, accounting for about 50 million deaths worldwide. In addition to a significant number of cases of secondary bacterial pneumonia, this highly pathogenic strain of influenza A virus caused fatal primary viral pneumonia. To identify the viral gene(s) chiefly responsible for the high virulence of the 1918 virus, we generated a series of reassortants between the 1918 virus and a contemporary human H1N1 virus (A/Kawasaki/173/2001; K173) using reverse genetics. We then assessed their virulence properties in ferrets, a model closely resembling humans in terms of sensitivity to influenza virus infection and pattern of spread after intranasal inoculation. Substitution of single genes from the 1918 virus in the genetic background of K173 virus did not markedly alter the pattern of infection. That is, the reassortants grew well in nasal turbinates, but only sporadically (if at all) in the trachea and lungs. One exception was the 1918PB1/K173 reassortant, which replicated efficiently in lung tissues as well as the upper respiratory tract. A reassortant virus expressing the 1918 viral RNA polymerase complex (PA, PB1, and PB2) and nucleoprotein showed virulence properties in the upper and lower respiratory tracts of ferrets that closely resembled those of wild-type 1918 virus. Our findings strongly implicate the viral RNA polymerase complex as a major determinant of the pathogenicity of the 1918 pandemic virus. This new insight may aid in identifying virulence factors in future pandemic viruses that could be targeted with antiviral compounds.</p>
</div>
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<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">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
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<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>Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Watanabe</surname>
<given-names>Tokiko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
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<contrib contrib-type="author"><name><surname>Watanabe</surname>
<given-names>Shinji</given-names>
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<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
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<contrib contrib-type="author"><name><surname>Shinya</surname>
<given-names>Kyoko</given-names>
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<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
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<contrib contrib-type="author"><name><surname>Kim</surname>
<given-names>Jin Hyun</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hatta</surname>
<given-names>Masato</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
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<contrib contrib-type="author"><name><surname>Kawaoka</surname>
<given-names>Yoshihiro</given-names>
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<xref ref-type="aff" rid="aff1"><sup>a</sup>
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<xref ref-type="aff" rid="aff2"><sup>b</sup>
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<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
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<aff id="aff1"><sup>a</sup>
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2015 Linden Drive, Madison, WI 53706;</aff>
<aff id="aff2"><sup>b</sup>
Division of Zoonosis, Department of Microbiology and Infectious Diseases, Graduate School of Medicine, Kobe University, Kobe 650-0017, Japan; and</aff>
<aff id="aff3"><sup>c</sup>
Division of Virology, Department of Microbiology and Immunology, and</aff>
<aff id="aff4"><sup>d</sup>
International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. E-Mail: <email>kawaokay@svm.vetmed.wisc.edu</email>
</corresp>
<fn fn-type="edited-by"><p>Edited by Hans-Dieter Klenk, Philipps-Universitat Marburg, Marburg, Germany, and accepted by the Editorial Board November 13, 2008</p>
</fn>
<fn fn-type="con"><p>Author contributions: T.W. and Y.K. designed research; T.W., S.W., K.S., J.H.K., and M.H. performed research; T.W., S.W., K.S., and Y.K. analyzed data; and T.W. and Y.K. wrote the paper.</p>
</fn>
<fn fn-type="conflict"><p>The authors declare no conflict of interest.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>13</day>
<month>1</month>
<year>2009</year>
</pub-date>
<pub-date pub-type="epub"><day>29</day>
<month>12</month>
<year>2008</year>
</pub-date>
<volume>106</volume>
<issue>2</issue>
<fpage>588</fpage>
<lpage>592</lpage>
<history><date date-type="received"><day>18</day>
<month>7</month>
<year>2008</year>
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<permissions><copyright-statement>© 2008 by The National Academy of Sciences of the USA</copyright-statement>
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<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="zpq00209000588.pdf"></self-uri>
<abstract><p>The 1918 influenza pandemic was the most devastating outbreak of infectious disease in human history, accounting for about 50 million deaths worldwide. In addition to a significant number of cases of secondary bacterial pneumonia, this highly pathogenic strain of influenza A virus caused fatal primary viral pneumonia. To identify the viral gene(s) chiefly responsible for the high virulence of the 1918 virus, we generated a series of reassortants between the 1918 virus and a contemporary human H1N1 virus (A/Kawasaki/173/2001; K173) using reverse genetics. We then assessed their virulence properties in ferrets, a model closely resembling humans in terms of sensitivity to influenza virus infection and pattern of spread after intranasal inoculation. Substitution of single genes from the 1918 virus in the genetic background of K173 virus did not markedly alter the pattern of infection. That is, the reassortants grew well in nasal turbinates, but only sporadically (if at all) in the trachea and lungs. One exception was the 1918PB1/K173 reassortant, which replicated efficiently in lung tissues as well as the upper respiratory tract. A reassortant virus expressing the 1918 viral RNA polymerase complex (PA, PB1, and PB2) and nucleoprotein showed virulence properties in the upper and lower respiratory tracts of ferrets that closely resembled those of wild-type 1918 virus. Our findings strongly implicate the viral RNA polymerase complex as a major determinant of the pathogenicity of the 1918 pandemic virus. This new insight may aid in identifying virulence factors in future pandemic viruses that could be targeted with antiviral compounds.</p>
</abstract>
<kwd-group><kwd>pathogenesis</kwd>
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