Complete and Incomplete Genome Packaging of Influenza A and B Viruses

ABSTRACT The genomes of influenza A and B viruses comprise eight segmented, single-stranded, negative-sense viral RNAs (vRNAs). Although segmentation of the virus genome complicates the packaging of infectious progeny into virions, it provides an evolutionary benefit in that it allows viruses to exc...

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Autores principales:	Sumiho Nakatsu, Hiroshi Sagara, Yuko Sakai-Tagawa, Norio Sugaya, Takeshi Noda, Yoshihiro Kawaoka
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2bf0de2f41d04505a9da3719e7060ffe
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spelling	oai:doaj.org-article:2bf0de2f41d04505a9da3719e7060ffe2021-11-15T15:50:15ZComplete and Incomplete Genome Packaging of Influenza A and B Viruses10.1128/mBio.01248-162150-7511https://doaj.org/article/2bf0de2f41d04505a9da3719e7060ffe2016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01248-16https://doaj.org/toc/2150-7511ABSTRACT The genomes of influenza A and B viruses comprise eight segmented, single-stranded, negative-sense viral RNAs (vRNAs). Although segmentation of the virus genome complicates the packaging of infectious progeny into virions, it provides an evolutionary benefit in that it allows viruses to exchange vRNAs with other strains. Influenza A viruses are believed to package their eight different vRNAs in a specific manner. However, several studies have shown that many viruses are noninfectious and fail to package at least one vRNA. Therefore, the genome-packaging mechanism is not fully understood. In this study, we used electron microscopy to count the number of ribonucleoproteins (RNPs) inside the virions of different influenza A and B virus strains. All eight strains examined displayed eight RNPs arranged in a “7+1” configuration in which a central RNP was surrounded by seven RNPs. Three-dimensional analysis of the virions showed that at least 80% of the virions packaged all eight RNPs; however, some virions packaged only five to seven RNPs, with the exact proportion depending on the strain examined. These results directly demonstrate that most viruses package eight RNPs, but some do indeed package fewer. Our findings support the selective genome-packaging model and demonstrate the variability in the number of RNPs incorporated by virions, suggesting that the genome-packaging mechanism of influenza viruses is more flexible than previously thought. IMPORTANCE The genomes of influenza A and B viruses contain segmented RNAs, which complicates genome packaging but provides the evolutionary advantage of allowing the exchange of individual genome segments with those of other strains. Some studies have shown that influenza A viruses package all eight genome segments in a specific manner, whereas others have shown that many virions are noninfectious and fail to package at least one genome segment. However, such viruses have never been directly observed. Here, we used electron microscopy to provide the first direct visual evidence of virions packaging an incomplete set of ribonucleoproteins. The percentage of these noninfectious virions varied from 0 to 20, depending on the virus strain, indicating that most virions package all eight genome segments. These results extend our knowledge about how infectious and noninfectious virions coordinate for successful virus infection.Sumiho NakatsuHiroshi SagaraYuko Sakai-TagawaNorio SugayaTakeshi NodaYoshihiro KawaokaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Sumiho Nakatsu Hiroshi Sagara Yuko Sakai-Tagawa Norio Sugaya Takeshi Noda Yoshihiro Kawaoka Complete and Incomplete Genome Packaging of Influenza A and B Viruses
description	ABSTRACT The genomes of influenza A and B viruses comprise eight segmented, single-stranded, negative-sense viral RNAs (vRNAs). Although segmentation of the virus genome complicates the packaging of infectious progeny into virions, it provides an evolutionary benefit in that it allows viruses to exchange vRNAs with other strains. Influenza A viruses are believed to package their eight different vRNAs in a specific manner. However, several studies have shown that many viruses are noninfectious and fail to package at least one vRNA. Therefore, the genome-packaging mechanism is not fully understood. In this study, we used electron microscopy to count the number of ribonucleoproteins (RNPs) inside the virions of different influenza A and B virus strains. All eight strains examined displayed eight RNPs arranged in a “7+1” configuration in which a central RNP was surrounded by seven RNPs. Three-dimensional analysis of the virions showed that at least 80% of the virions packaged all eight RNPs; however, some virions packaged only five to seven RNPs, with the exact proportion depending on the strain examined. These results directly demonstrate that most viruses package eight RNPs, but some do indeed package fewer. Our findings support the selective genome-packaging model and demonstrate the variability in the number of RNPs incorporated by virions, suggesting that the genome-packaging mechanism of influenza viruses is more flexible than previously thought. IMPORTANCE The genomes of influenza A and B viruses contain segmented RNAs, which complicates genome packaging but provides the evolutionary advantage of allowing the exchange of individual genome segments with those of other strains. Some studies have shown that influenza A viruses package all eight genome segments in a specific manner, whereas others have shown that many virions are noninfectious and fail to package at least one genome segment. However, such viruses have never been directly observed. Here, we used electron microscopy to provide the first direct visual evidence of virions packaging an incomplete set of ribonucleoproteins. The percentage of these noninfectious virions varied from 0 to 20, depending on the virus strain, indicating that most virions package all eight genome segments. These results extend our knowledge about how infectious and noninfectious virions coordinate for successful virus infection.
format	article
author	Sumiho Nakatsu Hiroshi Sagara Yuko Sakai-Tagawa Norio Sugaya Takeshi Noda Yoshihiro Kawaoka
author_facet	Sumiho Nakatsu Hiroshi Sagara Yuko Sakai-Tagawa Norio Sugaya Takeshi Noda Yoshihiro Kawaoka
author_sort	Sumiho Nakatsu
title	Complete and Incomplete Genome Packaging of Influenza A and B Viruses
title_short	Complete and Incomplete Genome Packaging of Influenza A and B Viruses
title_full	Complete and Incomplete Genome Packaging of Influenza A and B Viruses
title_fullStr	Complete and Incomplete Genome Packaging of Influenza A and B Viruses
title_full_unstemmed	Complete and Incomplete Genome Packaging of Influenza A and B Viruses
title_sort	complete and incomplete genome packaging of influenza a and b viruses
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/2bf0de2f41d04505a9da3719e7060ffe
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Complete and Incomplete Genome Packaging of Influenza A and B Viruses

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