The Avian-Origin PB1 Gene Segment Facilitated Replication and Transmissibility of the H3N2/1968 Pandemic Influenza Virus
Identifieur interne : 000031 ( 1957/Analysis ); précédent : 000030; suivant : 000032The Avian-Origin PB1 Gene Segment Facilitated Replication and Transmissibility of the H3N2/1968 Pandemic Influenza Virus
Auteurs : Isabel Wendel [Allemagne] ; Dennis Rubbenstroth [Allemagne] ; Jennifer Doedt [Allemagne] ; Georg Kochs [Allemagne] ; Jochen Wilhelm [Allemagne] ; Peter Staeheli [Allemagne] ; Hans-Dieter Klenk [Allemagne] ; Mikhail Matrosovich [Allemagne]Source :
- Journal of Virology [ 0022-538X ] ; 2015.
Descripteurs français
- KwdFr :
- Analyse de séquence d'ADN, Animaux, Cellules HEK293, Cellules rénales canines Madin-Darby, Chiens, Cochons d'Inde, Données de séquences moléculaires, Flambées de maladies (histoire), Grippe chez les oiseaux (transmission), Grippe chez les oiseaux (virologie), Grippe chez les oiseaux (épidémiologie), Grippe humaine (virologie), Grippe humaine (épidémiologie), Génétique inverse, Histoire du 20ème siècle, Humains, Modèles génétiques, Oiseaux, Phylogénie, Protéines virales (génétique), Protéines virales (physiologie), RT-PCR, Sous-type H3N2 du virus de la grippe A, Séquence nucléotidique, Zoonoses (transmission), Zoonoses (virologie), Zoonoses (épidémiologie).
- MESH :
- génétique : Protéines virales.
- histoire : Flambées de maladies.
- physiologie : Protéines virales.
- virologie : Grippe chez les oiseaux, Grippe humaine, Zoonoses.
- épidémiologie : Grippe chez les oiseaux, Grippe humaine, Zoonoses.
- Analyse de séquence d'ADN, Animaux, Cellules HEK293, Cellules rénales canines Madin-Darby, Chiens, Cochons d'Inde, Données de séquences moléculaires, Génétique inverse, Histoire du 20ème siècle, Humains, Modèles génétiques, Oiseaux, Phylogénie, RT-PCR, Sous-type H3N2 du virus de la grippe A, Séquence nucléotidique.
English descriptors
- KwdEn :
- Animals, Base Sequence, Birds, Disease Outbreaks (history), Dogs, Guinea Pigs, HEK293 Cells, History, 20th Century, Humans, Influenza A Virus, H3N2 Subtype, Influenza in Birds (epidemiology), Influenza in Birds (transmission), Influenza in Birds (virology), Influenza, Human (epidemiology), Influenza, Human (virology), Madin Darby Canine Kidney Cells, Models, Genetic, Molecular Sequence Data, Phylogeny, Reverse Genetics, Reverse Transcriptase Polymerase Chain Reaction, Sequence Analysis, DNA, Viral Proteins (genetics), Viral Proteins (physiology), Zoonoses (epidemiology), Zoonoses (transmission), Zoonoses (virology).
- MESH :
- chemical , genetics : Viral Proteins.
- epidemiology : Influenza in Birds, Influenza, Human, Zoonoses.
- history : Disease Outbreaks.
- chemical , physiology : Viral Proteins.
- transmission : Influenza in Birds, Zoonoses.
- virology : Influenza in Birds, Influenza, Human, Zoonoses.
- Animals, Base Sequence, Birds, Dogs, Guinea Pigs, HEK293 Cells, History, 20th Century, Humans, Influenza A Virus, H3N2 Subtype, Madin Darby Canine Kidney Cells, Models, Genetic, Molecular Sequence Data, Phylogeny, Reverse Genetics, Reverse Transcriptase Polymerase Chain Reaction, Sequence Analysis, DNA.
Abstract
The H2N2/1957 and H3N2/1968 pandemic influenza viruses emerged via the exchange of genomic RNA segments between human and avian viruses. The avian hemagglutinin (HA) allowed the hybrid viruses to escape preexisting immunity in the human population. Both pandemic viruses further received the PB1 gene segment from the avian parent (Y. Kawaoka, S. Krauss, and R. G. Webster, J Virol 63:4603–4608, 1989), but the biological significance of this observation was not understood. To assess whether the avian-origin PB1 segment provided pandemic viruses with some selective advantage, either on its own or via cooperation with the homologous HA segment, we modeled by reverse genetics the reassortment event that led to the emergence of the H3N2/1968 pandemic virus. Using seasonal H2N2 virus A/California/1/66 (Cal) as a surrogate precursor human virus and pandemic virus A/Hong Kong/1/68 (H3N2) (HK) as a source of avian-derived PB1 and HA gene segments, we generated four reassortant recombinant viruses and compared pairs of viruses which differed solely by the origin of PB1. Replacement of the PB1 segment of Cal by PB1 of HK facilitated viral polymerase activity, replication efficiency in human cells, and contact transmission in guinea pigs. A combination of PB1 and HA segments of HK did not enhance replicative fitness of the reassortant virus compared with the single-gene PB1 reassortant. Our data suggest that the avian PB1 segment of the 1968 pandemic virus served to enhance viral growth and transmissibility, likely by enhancing activity of the viral polymerase complex.
Url:
DOI: 10.1128/JVI.03194-14
PubMed: 25631088
PubMed Central: 4442368
Affiliations:
- Allemagne
- Bade-Wurtemberg, District de Fribourg-en-Brisgau, District de Giessen, Hesse (Land)
- Fribourg-en-Brisgau, Marbourg
Links toward previous steps (curation, corpus...)
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Links to Exploration step
PMC:4442368Le document en format XML
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<term>Base Sequence</term>
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<term>Dogs</term>
<term>Guinea Pigs</term>
<term>HEK293 Cells</term>
<term>History, 20th Century</term>
<term>Humans</term>
<term>Influenza A Virus, H3N2 Subtype</term>
<term>Influenza in Birds (epidemiology)</term>
<term>Influenza in Birds (transmission)</term>
<term>Influenza in Birds (virology)</term>
<term>Influenza, Human (epidemiology)</term>
<term>Influenza, Human (virology)</term>
<term>Madin Darby Canine Kidney Cells</term>
<term>Models, Genetic</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Reverse Genetics</term>
<term>Reverse Transcriptase Polymerase Chain Reaction</term>
<term>Sequence Analysis, DNA</term>
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<term>Zoonoses (transmission)</term>
<term>Zoonoses (virology)</term>
</keywords>
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<term>Animaux</term>
<term>Cellules HEK293</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Cochons d'Inde</term>
<term>Données de séquences moléculaires</term>
<term>Flambées de maladies (histoire)</term>
<term>Grippe chez les oiseaux (transmission)</term>
<term>Grippe chez les oiseaux (virologie)</term>
<term>Grippe chez les oiseaux (épidémiologie)</term>
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<term>Grippe humaine (épidémiologie)</term>
<term>Génétique inverse</term>
<term>Histoire du 20ème siècle</term>
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<term>Oiseaux</term>
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<term>Grippe humaine</term>
<term>Zoonoses</term>
</keywords>
<keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Influenza in Birds</term>
<term>Influenza, Human</term>
<term>Zoonoses</term>
</keywords>
<keywords scheme="MESH" qualifier="épidémiologie" xml:lang="fr"><term>Grippe chez les oiseaux</term>
<term>Grippe humaine</term>
<term>Zoonoses</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Base Sequence</term>
<term>Birds</term>
<term>Dogs</term>
<term>Guinea Pigs</term>
<term>HEK293 Cells</term>
<term>History, 20th Century</term>
<term>Humans</term>
<term>Influenza A Virus, H3N2 Subtype</term>
<term>Madin Darby Canine Kidney Cells</term>
<term>Models, Genetic</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Reverse Genetics</term>
<term>Reverse Transcriptase Polymerase Chain Reaction</term>
<term>Sequence Analysis, DNA</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Analyse de séquence d'ADN</term>
<term>Animaux</term>
<term>Cellules HEK293</term>
<term>Cellules rénales canines Madin-Darby</term>
<term>Chiens</term>
<term>Cochons d'Inde</term>
<term>Données de séquences moléculaires</term>
<term>Génétique inverse</term>
<term>Histoire du 20ème siècle</term>
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</teiHeader>
<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>The H2N2/1957 and H3N2/1968 pandemic influenza viruses emerged via the exchange of genomic RNA segments between human and avian viruses. The avian hemagglutinin (HA) allowed the hybrid viruses to escape preexisting immunity in the human population. Both pandemic viruses further received the PB1 gene segment from the avian parent (Y. Kawaoka, S. Krauss, and R. G. Webster, J Virol 63:4603–4608, 1989), but the biological significance of this observation was not understood. To assess whether the avian-origin PB1 segment provided pandemic viruses with some selective advantage, either on its own or via cooperation with the homologous HA segment, we modeled by reverse genetics the reassortment event that led to the emergence of the H3N2/1968 pandemic virus. Using seasonal H2N2 virus A/California/1/66 (Cal) as a surrogate precursor human virus and pandemic virus A/Hong Kong/1/68 (H3N2) (HK) as a source of avian-derived PB1 and HA gene segments, we generated four reassortant recombinant viruses and compared pairs of viruses which differed solely by the origin of PB1. Replacement of the PB1 segment of Cal by PB1 of HK facilitated viral polymerase activity, replication efficiency in human cells, and contact transmission in guinea pigs. A combination of PB1 and HA segments of HK did not enhance replicative fitness of the reassortant virus compared with the single-gene PB1 reassortant. Our data suggest that the avian PB1 segment of the 1968 pandemic virus served to enhance viral growth and transmissibility, likely by enhancing activity of the viral polymerase complex.
</p>
<p><bold>IMPORTANCE</bold>
Despite the high impact of influenza pandemics on human health, some mechanisms underlying the emergence of pandemic influenza viruses still are poorly understood. Thus, it was unclear why both H2N2/1957 and H3N2/1968 reassortant pandemic viruses contained, in addition to the avian HA, the PB1 gene segment of the avian parent. Here, we addressed this long-standing question by modeling the emergence of the H3N2/1968 virus from its putative human and avian precursors. We show that the avian PB1 segment increased activity of the viral polymerase and facilitated viral replication. Our results suggest that in addition to the acquisition of antigenically novel HA (i.e., antigenic shift), enhanced viral polymerase activity is required for the emergence of pandemic influenza viruses from their seasonal human precursors.</p>
</div>
</front>
</TEI>
<affiliations><list><country><li>Allemagne</li>
</country>
<region><li>Bade-Wurtemberg</li>
<li>District de Fribourg-en-Brisgau</li>
<li>District de Giessen</li>
<li>Hesse (Land)</li>
</region>
<settlement><li>Fribourg-en-Brisgau</li>
<li>Marbourg</li>
</settlement>
</list>
<tree><country name="Allemagne"><region name="Hesse (Land)"><name sortKey="Wendel, Isabel" sort="Wendel, Isabel" uniqKey="Wendel I" first="Isabel" last="Wendel">Isabel Wendel</name>
</region>
<name sortKey="Doedt, Jennifer" sort="Doedt, Jennifer" uniqKey="Doedt J" first="Jennifer" last="Doedt">Jennifer Doedt</name>
<name sortKey="Klenk, Hans Dieter" sort="Klenk, Hans Dieter" uniqKey="Klenk H" first="Hans-Dieter" last="Klenk">Hans-Dieter Klenk</name>
<name sortKey="Kochs, Georg" sort="Kochs, Georg" uniqKey="Kochs G" first="Georg" last="Kochs">Georg Kochs</name>
<name sortKey="Matrosovich, Mikhail" sort="Matrosovich, Mikhail" uniqKey="Matrosovich M" first="Mikhail" last="Matrosovich">Mikhail Matrosovich</name>
<name sortKey="Rubbenstroth, Dennis" sort="Rubbenstroth, Dennis" uniqKey="Rubbenstroth D" first="Dennis" last="Rubbenstroth">Dennis Rubbenstroth</name>
<name sortKey="Staeheli, Peter" sort="Staeheli, Peter" uniqKey="Staeheli P" first="Peter" last="Staeheli">Peter Staeheli</name>
<name sortKey="Wilhelm, Jochen" sort="Wilhelm, Jochen" uniqKey="Wilhelm J" first="Jochen" last="Wilhelm">Jochen Wilhelm</name>
</country>
</tree>
</affiliations>
</record>
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