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M gene reassortment in H9N2 influenza virus promotes early infection and replication: contribution to rising virus prevalence in chickens in China

Pu, Juan; Sun, Honglei; Qu, Yi; Wang, Chenxi; Gao, Weihua; Zhu, Junda; Sun, Yipeng; Bi, Yuhai; Huang, Yinhua; Chang, Kin-Chow; Cui, Jie; Liu, Jinhua

M gene reassortment in H9N2 influenza virus promotes early infection and replication: contribution to rising virus prevalence in chickens in China Thumbnail


Authors

Juan Pu

Honglei Sun

Yi Qu

Chenxi Wang

Weihua Gao

Junda Zhu

Yipeng Sun

Yuhai Bi

Yinhua Huang

KIN-CHOW CHANG KIN-CHOW.CHANG@NOTTINGHAM.AC.UK
Professor of Veterinary Molecular Medicine

Jie Cui

Jinhua Liu



Abstract

Segment reassortment and base mutagenesis of influenza A viruses are the primary routes to the rapid evolution of high fitness virus genotypes. We recently described a predominant G57 genotype of avian H9N2 viruses that caused country-wide outbreaks in chickens in China during 2010-2013 which led to the zoonotic emergence of H7N9 viruses. One of the key features of the G57 genotype is the substitution of the earlier BJ/94-like M gene with the G1-like M gene of quail origin. We report here on the functional significance of the G1-like M gene in H9N2 viruses in conferring increased infection severity and infectivity in primary chicken embryonic fibroblasts and chickens. H9N2 virus housing the G1-like M gene, in place of BJ/94-like M gene, showed early surge in viral mRNA and vRNA transcription that were associated with enhanced viral protein production, and with early elevated release of progeny virus comprising largely spherical rather than filamentous virions. Importantly, H9N2 virus with G1-like M gene conferred extrapulmonary virus spread in chickens. Five highly represented signature amino acid residues (37A, 95K, 224N and 242N in M1 protein, and 21G in M2 protein) encoded by the prevalent G1-like M gene were demonstrated as prime contributors to enhanced infectivity. Therefore, the genetic evolution of M gene in H9N2 virus increases reproductive virus fitness, indicating its contribution to rising virus prevalence in chickens in China.

Importance We recently described the circulation of a dominant genotype (G57) of H9N2 viruses in country-wide outbreaks in chickens in China, which was responsible through reassortment for the emergence of H7N9 viruses that cause severe human infections. A key feature of the G57 genotype H9N2 virus is the presence of quail origin G1-like M gene which had replaced the earlier BJ/94-like M gene. We found that H9N2 virus with G1-like M gene, but not BJ/94-like M gene, showed early surge in progeny virus production, more severe pathology and extrapulmonary virus spread in chickens. Five highly represented amino acid residues in M1 and M2 proteins derived from G1-like M gene were shown to mediate enhanced virus infectivity. These observations enhance what we currently know about the roles of reassortment and mutations on virus fitness and have implications for assessing the potential of variant influenza viruses that can cause rising prevalence in chickens.

Citation

Pu, J., Sun, H., Qu, Y., Wang, C., Gao, W., Zhu, J., …Liu, J. (2017). M gene reassortment in H9N2 influenza virus promotes early infection and replication: contribution to rising virus prevalence in chickens in China. Journal of Virology, 91(8), Article e02055-16. https://doi.org/10.1128/JVI.02055-16

Journal Article Type Article
Acceptance Date Jan 25, 2017
Online Publication Date Feb 1, 2017
Publication Date Apr 1, 2017
Deposit Date Feb 2, 2017
Publicly Available Date Mar 28, 2024
Journal Journal of Virology
Print ISSN 0022-538X
Electronic ISSN 1098-5514
Publisher American Society for Microbiology
Peer Reviewed Peer Reviewed
Volume 91
Issue 8
Article Number e02055-16
DOI https://doi.org/10.1128/JVI.02055-16
Keywords chicken, H9N2 virus, M gene, reassortment, replication
Public URL https://nottingham-repository.worktribe.com/output/854013
Publisher URL http://jvi.asm.org/content/91/8/e02055-16

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