Influenza NA and PB1 Gene Segments Interact during the Formation of Viral Progeny: Localization of the Binding Region within the PB1 Gene
Identifieur interne : 000074 ( France/Analysis ); précédent : 000073; suivant : 000075Influenza NA and PB1 Gene Segments Interact during the Formation of Viral Progeny: Localization of the Binding Region within the PB1 Gene
Auteurs : Brad Gilbertson ; Tian Zheng ; Marie Gerber ; Anne Printz-Schweigert ; Chi Ong ; Roland Marquet ; Catherine Isel [France] ; Steven Rockman ; Lorena BrownSource :
- Viruses [ 1999-4915 ] ; 2016.
Abstract
The influenza A virus genome comprises eight negative-sense viral RNAs (vRNAs) that form individual ribonucleoprotein (RNP) complexes. In order to incorporate a complete set of each of these vRNAs, the virus uses a selective packaging mechanism that facilitates co-packaging of specific gene segments but whose molecular basis is still not fully understood. Recently, we used a competitive transfection model where plasmids encoding the A/Puerto Rico/8/34 (PR8) and A/Udorn/307/72 (Udorn) PB1 gene segments were competed to show that the Udorn PB1 gene segment is preferentially co-packaged into progeny virions with the Udorn NA gene segment. Here we created chimeric PB1 genes combining both Udorn and PR8 PB1 sequences to further define the location within the Udorn PB1 gene that drives co-segregation of these genes and show that nucleotides 1776–2070 of the PB1 gene are crucial for preferential selection. In vitro assays examining specific interactions between Udorn NA vRNA and purified vRNAs transcribed from chimeric PB1 genes also supported the importance of this region in the PB1-NA interaction. Hence, this work identifies an association between viral genes that are co-selected during packaging. It also reveals a region potentially important in the RNP-RNP interactions within the supramolecular complex that is predicted to form prior to budding to allow one of each segment to be packaged in the viral progeny. Our study lays the foundation to understand the co-selection of specific genes, which may be critical to the emergence of new viruses with pandemic potential.
Url:
DOI: 10.3390/v8080238
PubMed: 27556479
PubMed Central: 4997600
Affiliations:
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PMC:4997600Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Influenza NA and PB1 Gene Segments Interact during the Formation of Viral Progeny: Localization of the Binding Region within the PB1 Gene</title><author><name sortKey="Gilbertson, Brad" sort="Gilbertson, Brad" uniqKey="Gilbertson B" first="Brad" last="Gilbertson">Brad Gilbertson</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation></author><author><name sortKey="Zheng, Tian" sort="Zheng, Tian" uniqKey="Zheng T" first="Tian" last="Zheng">Tian Zheng</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation></author><author><name sortKey="Gerber, Marie" sort="Gerber, Marie" uniqKey="Gerber M" first="Marie" last="Gerber">Marie Gerber</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation></author><author><name sortKey="Printz Schweigert, Anne" sort="Printz Schweigert, Anne" uniqKey="Printz Schweigert A" first="Anne" last="Printz-Schweigert">Anne Printz-Schweigert</name><affiliation><nlm:aff 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France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation></author><author><name sortKey="Isel, Catherine" sort="Isel, Catherine" uniqKey="Isel C" first="Catherine" last="Isel">Catherine Isel</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation><affiliation wicri:level="3"><nlm:aff id="af4-viruses-08-00238">Unité de Génétique Moléculaire des Virus à ARN, Département de virologie, Institut Pasteur, Paris 75005, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Unité de Génétique Moléculaire des Virus à ARN, Département de virologie, Institut Pasteur, Paris 75005</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Rockman, Steven" sort="Rockman, Steven" uniqKey="Rockman S" first="Steven" last="Rockman">Steven Rockman</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation><affiliation><nlm:aff id="af3-viruses-08-00238">Seqirus, 63 Poplar Rd, Parkville 3052, Victoria, Australia;<email>Chi.Ong@seqirus.com</email></nlm:aff></affiliation></author><author><name sortKey="Brown, Lorena" sort="Brown, 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Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation></author><author><name sortKey="Zheng, Tian" sort="Zheng, Tian" uniqKey="Zheng T" first="Tian" last="Zheng">Tian Zheng</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation></author><author><name sortKey="Gerber, Marie" sort="Gerber, Marie" uniqKey="Gerber M" first="Marie" last="Gerber">Marie Gerber</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation></author><author><name sortKey="Printz Schweigert, Anne" sort="Printz Schweigert, Anne" uniqKey="Printz Schweigert A" first="Anne" last="Printz-Schweigert">Anne Printz-Schweigert</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation></author><author><name sortKey="Ong, Chi" sort="Ong, Chi" uniqKey="Ong C" first="Chi" last="Ong">Chi Ong</name><affiliation><nlm:aff id="af3-viruses-08-00238">Seqirus, 63 Poplar Rd, Parkville 3052, Victoria, Australia;<email>Chi.Ong@seqirus.com</email></nlm:aff></affiliation></author><author><name sortKey="Marquet, Roland" sort="Marquet, Roland" uniqKey="Marquet R" first="Roland" last="Marquet">Roland Marquet</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation></author><author><name sortKey="Isel, Catherine" sort="Isel, Catherine" uniqKey="Isel C" first="Catherine" last="Isel">Catherine Isel</name><affiliation><nlm:aff id="af2-viruses-08-00238">Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, Strasbourg 67084, France;<email>m.gerber@ibmc-cnrs.unistra.fr</email> (M.G.);<email>A.schweigert@ibmc-cnrs.unistra.fr</email> (A.P.-S.);<email>r.marquet@ibmc-cnrs.unistra.fr</email> (R.M.);<email>c.isel@ibmc-cnrs.unistra.fr</email> (C.I.)</nlm:aff></affiliation><affiliation wicri:level="3"><nlm:aff id="af4-viruses-08-00238">Unité de Génétique Moléculaire des Virus à ARN, Département de virologie, Institut Pasteur, Paris 75005, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Unité de Génétique Moléculaire des Virus à ARN, Département de virologie, Institut Pasteur, Paris 75005</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Rockman, Steven" sort="Rockman, Steven" uniqKey="Rockman S" first="Steven" last="Rockman">Steven Rockman</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation><affiliation><nlm:aff id="af3-viruses-08-00238">Seqirus, 63 Poplar Rd, Parkville 3052, Victoria, Australia;<email>Chi.Ong@seqirus.com</email></nlm:aff></affiliation></author><author><name sortKey="Brown, Lorena" sort="Brown, Lorena" uniqKey="Brown L" first="Lorena" last="Brown">Lorena Brown</name><affiliation><nlm:aff id="af1-viruses-08-00238">Department of Microbiology and Immunology, The University of Melbourne at the Peter Doherty Institute of Infection and Immunity, Parkville 3010, Victoria, Australia;<email>bg@unimelb.edu.au</email> (B.G.);<email>tianchi.zheng@gmail.com</email> (T.Z.);<email>Steve.Rockman@seqirus.com</email> (S.R.)</nlm:aff></affiliation></author></analytic><series><title level="j">Viruses</title><idno type="eISSN">1999-4915</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The influenza A virus genome comprises eight negative-sense viral RNAs (vRNAs) that form individual ribonucleoprotein (RNP) complexes. In order to incorporate a complete set of each of these vRNAs, the virus uses a selective packaging mechanism that facilitates co-packaging of specific gene segments but whose molecular basis is still not fully understood. Recently, we used a competitive transfection model where plasmids encoding the A/Puerto Rico/8/34 (PR8) and A/Udorn/307/72 (Udorn) PB1 gene segments were competed to show that the Udorn PB1 gene segment is preferentially co-packaged into progeny virions with the Udorn NA gene segment. Here we created chimeric PB1 genes combining both Udorn and PR8 PB1 sequences to further define the location within the Udorn PB1 gene that drives co-segregation of these genes and show that nucleotides 1776–2070 of the PB1 gene are crucial for preferential selection. In vitro assays examining specific interactions between Udorn NA vRNA and purified vRNAs transcribed from chimeric PB1 genes also supported the importance of this region in the PB1-NA interaction. Hence, this work identifies an association between viral genes that are co-selected during packaging. It also reveals a region potentially important in the RNP-RNP interactions within the supramolecular complex that is predicted to form prior to budding to allow one of each segment to be packaged in the viral progeny. Our study lays the foundation to understand the co-selection of specific genes, which may be critical to the emergence of new viruses with pandemic potential.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hsu, M T" uniqKey="Hsu M">M.T. Hsu</name></author><author><name sortKey="Parvin, J D" uniqKey="Parvin J">J.D. Parvin</name></author><author><name sortKey="Gupta, S" uniqKey="Gupta S">S. Gupta</name></author><author><name sortKey="Krystal, M" uniqKey="Krystal M">M. Krystal</name></author><author><name sortKey="Palese, P" uniqKey="Palese P">P. 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Rott</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chen, W" uniqKey="Chen W">W. Chen</name></author><author><name sortKey="Calvo, P A" uniqKey="Calvo P">P.A. Calvo</name></author><author><name sortKey="Malide, D" uniqKey="Malide D">D. Malide</name></author><author><name sortKey="Gibbs, J" uniqKey="Gibbs J">J. Gibbs</name></author><author><name sortKey="Schubert, U" uniqKey="Schubert U">U. Schubert</name></author><author><name sortKey="Bacik, I" uniqKey="Bacik I">I. Bacik</name></author><author><name sortKey="Basta, S" uniqKey="Basta S">S. Basta</name></author><author><name sortKey="O Eill, R" uniqKey="O Eill R">R. O‘Neill</name></author><author><name sortKey="Schickli, J" uniqKey="Schickli J">J. Schickli</name></author><author><name sortKey="Palese, P" uniqKey="Palese P">P. Palese</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mcauley, J L" uniqKey="Mcauley J">J.L. McAuley</name></author><author><name sortKey="Tate, M D" uniqKey="Tate M">M.D. Tate</name></author><author><name sortKey="Mackenzie Kludas, C J" uniqKey="Mackenzie Kludas C">C.J. MacKenzie-Kludas</name></author><author><name sortKey="Pinar, A" uniqKey="Pinar A">A. Pinar</name></author><author><name sortKey="Zeng, W" uniqKey="Zeng W">W. Zeng</name></author><author><name sortKey="Stutz, A" uniqKey="Stutz A">A. Stutz</name></author><author><name sortKey="Latz, E" uniqKey="Latz E">E. Latz</name></author><author><name sortKey="Brown, L E" uniqKey="Brown L">L.E. Brown</name></author><author><name sortKey="Mansell, A" uniqKey="Mansell A">A. Mansell</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li></country><region><li>Île-de-France</li></region></list><tree><noCountry><name sortKey="Brown, Lorena" sort="Brown, Lorena" uniqKey="Brown L" first="Lorena" last="Brown">Lorena Brown</name><name sortKey="Gerber, Marie" sort="Gerber, Marie" uniqKey="Gerber M" first="Marie" last="Gerber">Marie Gerber</name><name sortKey="Gilbertson, Brad" sort="Gilbertson, Brad" uniqKey="Gilbertson B" first="Brad" last="Gilbertson">Brad Gilbertson</name><name sortKey="Marquet, Roland" sort="Marquet, Roland" uniqKey="Marquet R" first="Roland" last="Marquet">Roland Marquet</name><name sortKey="Ong, Chi" sort="Ong, Chi" uniqKey="Ong C" first="Chi" last="Ong">Chi Ong</name><name sortKey="Printz Schweigert, Anne" sort="Printz Schweigert, Anne" uniqKey="Printz Schweigert A" first="Anne" last="Printz-Schweigert">Anne Printz-Schweigert</name><name sortKey="Rockman, Steven" sort="Rockman, Steven" uniqKey="Rockman S" first="Steven" last="Rockman">Steven Rockman</name><name sortKey="Zheng, Tian" sort="Zheng, Tian" uniqKey="Zheng T" first="Tian" last="Zheng">Tian Zheng</name></noCountry><country name="France"><region name="Île-de-France"><name sortKey="Isel, Catherine" sort="Isel, Catherine" uniqKey="Isel C" first="Catherine" last="Isel">Catherine Isel</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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