The PB2 and M genes of genotype S H9N2 virus contribute to the enhanced fitness of H5Nx and H7N9 avian influenza viruses in chickens

Hao, Xiaoli; Wang, Xiaoquan; Hu, Jiao; Gu, Minghong; Wang, Danny J.J.; Deng, Yifan; Jiang, Daxiu; He, Deqin; Xu, Haixu; Yang, Yi; Hu, Zenglei; Chen, Sujuan; Hu, Shunlin; Liu, Xiaowen; Shang, Shaobin; Peng, Daxin; Jiao, Xinan

doi:10.1016/j.virol.2019.07.001

Cited by 15 publications

(16 citation statements)

References 33 publications

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“…The enhanced fitness of genotype S in chickens is partly attributable to the acquisition of G1/97-like MP and PB2 genes. These genes increase AIV polymerase activity, replicative capacity, and virulence of AIVs in chickens [91,92]. Both Cambodian genotype P and V viruses contained G1/97-like matrix proteins, but only genotype V also has a G1/97-like PB2.…”

Section: Discussionmentioning

confidence: 99%

The evolution and genetic diversity of avian influenza A(H9N2) viruses in Cambodia, 2015 – 2016

et al. 2019

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Low pathogenic A(H9N2) subtype avian influenza viruses (AIVs) were originally detected in Cambodian poultry in 2013, and now circulate endemically. We sequenced and characterised 64 A(H9N2) AIVs detected in Cambodian poultry (chickens and ducks) from January 2015 to May 2016. All A(H9) viruses collected in 2015 and 2016 belonged to a new BJ/94-like h9-4.2.5 sub-lineage that emerged in the region during or after 2013, and was distinct to previously detected Cambodian viruses. Overall, there was a reduction of genetic diversity of H9N2 since 2013, however two genotypes were detected in circulation, P and V, with extensive reassortment between the viruses. Phylogenetic analysis showed a close relationship between A(H9N2) AIVs detected in Cambodian and Vietnamese poultry, highlighting cross-border trade/movement of live, domestic poultry between the countries. Wild birds may also play a role in A(H9N2) transmission in the region. Some genes of the Cambodian isolates frequently clustered with zoonotic A(H7N9), A(H9N2) and A(H10N8) viruses, suggesting a common ecology. Molecular analysis showed 100% of viruses contained the hemagglutinin (HA) Q226L substitution, which favours mammalian receptor type binding. All viruses were susceptible to the neuraminidase inhibitor antivirals; however, 41% contained the matrix (M2) S31N substitution associated with resistance to adamantanes. Overall, Cambodian A(H9N2) viruses possessed factors known to increase zoonotic potential, and therefore their evolution should be continually monitored.

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Section: Discussionmentioning

confidence: 99%

The evolution and genetic diversity of avian influenza A(H9N2) viruses in Cambodia, 2015 – 2016

et al. 2019

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“…Viruses A/chicken/Guangdong/GD15/2016 (GD/15, H7N9), A/chicken/Jiangsu/YB7/2015 (YB/7, clade 2.3.2.1 H5N1), A/goose/Jiangsu/QD5/2014 (QD/5, H5N8), A/chicken/Anhui/QD1/2014 (QD/1, clade 2.3.4.4 H5N1), A/Chicken/Jiangsu/CZ/73/2014 (CZ/73, genotype S H9N2) and A/chicken/Shanghai/14/2001 (SH/14, genotype H H9N2), which have been described previously (Hao et al, ; Liu et al, ; Zhang et al, ), were used in this study. The accession numbers and genotypes of the original internal genes of these viruses have been described previously (Hao et al, ). Virus stocks were grown in 9‐ to 10‐day‐old specific‐pathogen‐free (SPF) chicken eggs.…”

Section: Methodsmentioning

confidence: 99%

“…(Hao et al, 2017;Liu et al, 2018;Zhang et al, 2008), were used in this study. The accession numbers and genotypes of the original internal genes of these viruses have been described previously (Hao et al, 2019). Virus stocks were grown in 9-to 10-day-old specific-pathogen-free (SPF) chicken eggs.…”

Section: Ethic Statementsmentioning

confidence: 99%

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The PB2 and M genes are critical for the superiority of genotype S H9N2 virus to genotype H in optimizing viral fitness of H5Nx and H7N9 avian influenza viruses in mice

Hao

Wang

et al. 2019

Transbound Emerg Dis

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Genotype S H9N2 avian influenza virus, which has been predominant in China since 2010, contributed its entire internal gene cassette to the genesis of novel reassortant influenza viruses, including H5Nx, H7N9 and H10N8 viruses that pose great threat to poultry and humans. A key feature of the genotype S H9N2 virus is the substitution of G1‐like M and PB2 genes for the earlier F/98‐like M and PB2 of genotype H virus. However, how this gene substitution has influenced viral adaptability of emerging influenza viruses in mammals remains unclear. We report here that reassortant H5Nx and H7N9 viruses with the genotype S internal gene cassette displayed enhanced replication and virulence over those with genotype H internal gene cassette in cell cultures as well as in the mouse models. We showed that the G1‐like PB2 gene was associated with increased polymerase activity and improved nuclear accumulation compared with the F/98‐like counterpart, while the G1‐like M gene facilitated effective translocation of RNP to cytoplasm. Our findings suggest that the genotype S H9N2 internal gene cassette, which possesses G1‐like M and PB2 genes, is superior to that of genotype H, in optimizing viral fitness, and thus have implications for assessing the potential risk of these gene introductions to generate emerging influenza viruses.

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“…The S genotype, which differs from F/98-like viruses (genotype H) only in their M and PB2 genes [11,12], has not been replaced by a new genotype since 2010 [2]. As S genotype viruses carry the genetic backbone of F/ 98-like viruses (genotype H) plus the M and PB2 genes of the G1-like viruses, it is presumed that the G1-like M and PB2 genes confer better viral fitness over F/98-like counterparts.…”

Section: Introductionmentioning

confidence: 99%

G1-like M and PB2 genes are preferentially incorporated into H7N9 progeny virions during genetic reassortment

Wang

et al. 2021

BMC Vet Res

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Background Genotype S H9N2 viruses have become predominant in poultry in China since 2010. These viruses frequently donate their whole internal gene segments to other emerging influenza A subtypes such as the novel H7N9, H5N6, and H10N8 viruses. We recently reported that the PB2 and M genes of the genotype S H9N2 virus, which are derived from the G1-like virus, enhance the fitness of H5Nx and H7N9 avian influenza viruses in chickens and mice. However, whether the G1-like PB2 and M genes are preferentially incorporated into progeny virions during virus reassortment remains unclear; whether the G1-like PB2 and M genes from different subtypes are differentially incorporated into new virion progeny remains unknown. Results We conducted a reassortment experiment with the use of a H7N9 virus as the backbone and found that G1-like M/PB2 genes were preferentially incorporated in progeny virions over F/98-like M/PB2 genes. Importantly, the preference varied among G1-like M/PB2 genes of different subtypes. When competing with F/98-like M/PB2 genes during reassortment, both the M and PB2 genes from the H7N9 virus GD15 showed an advantage, whereas only the PB2 gene from the H9N2 virus CZ73 and the M gene from the H9N2 virus AH320 displayed the advantage. Conclusion Our findings highlight the preferential and variable advantages of H9N2-derived G1-like M and PB2 genes in incorporating them into H7N9 progeny virions over SH14-derived F/98-like M/PB2 genes.

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The PB2 and M genes of genotype S H9N2 virus contribute to the enhanced fitness of H5Nx and H7N9 avian influenza viruses in chickens

Cited by 15 publications

References 33 publications

The evolution and genetic diversity of avian influenza A(H9N2) viruses in Cambodia, 2015 – 2016

The evolution and genetic diversity of avian influenza A(H9N2) viruses in Cambodia, 2015 – 2016

The PB2 and M genes are critical for the superiority of genotype S H9N2 virus to genotype H in optimizing viral fitness of H5Nx and H7N9 avian influenza viruses in mice

G1-like M and PB2 genes are preferentially incorporated into H7N9 progeny virions during genetic reassortment

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