Research Article: Genetic and biological characterization of H9N2 avian influenza viruses isolated in China from 2011 to 2014

Date Published: July 3, 2018

Publisher: Public Library of Science

Author(s): Rui Zhu, Danwen Xu, Xueqin Yang, Jianjun Zhang, Shifeng Wang, Huoying Shi, Xiufan Liu, Florian Krammer.


The genotypes of the H9N2 avian influenza viruses have changed since 2013 when almost all H9N2 viruses circulating in chickens in China were genotype 57 (G57) with the fittest lineage of each gene. To characterize the H9N2 variant viruses from 2011 to 2014, 28 H9N2 influenza viruses were isolated from live poultry markets in China from 2011–2014 and were analyzed by genetic and biological characterization. Our findings showed that 16 residues that changed antigenicity, two potential N-linked glycosylation sites, and one amino acid in the receptor binding site of the HA protein changed significantly from 2011–2014. Moreover, the HA and NA genes in the phylogenetic tree were mainly clustered into two independent branches, A and B, based on the year of isolation. H9N2 virus internal genes were related to those from the human-infected avian influenza viruses H5N1, H7N9, and H10N8. In particular, the NS gene in the phylogenetic tree revealed genetic divergence of the virus gene into three branches labeled A, B, and C, which were related to the H9N2, H10N8, and H7N9 viruses, respectively. Additionally, the isolates also showed varying levels of infection and airborne transmission. These results indicated that the H9N2 virus had undergone an adaptive evolution and variation from 2011–2014.

Partial Text

The subtype H9N2 low-pathogenic avian influenza viruses have been prevalent in China since 1994. H9N2 viruses can cause great economic losses to the domestic poultry industry when co-infected with H5 or H7 influenza viruses or other pathogens including Escherichia coli, Chlamydia psittaci, Ornithobacterium rhinotracheale, Staphylococcus aureus, Haemophilus paragallinarum and others [1–5]. Aside from waterfowl and poultry, different mammalian hosts, including humans, have been infected with H9N2 influenza viruses [6–9]. Additionally, H9N2 viruses also contribute to the reassortment of other virus subtypes, such as the human-infected H5N1 and H7N9 viruses and the emerging avian influenza viruses H6N1 and H10N8 [10–14]. Therefore, H9N2 viruses have become a potential threat to public health.

H9N2 subtype avian influenza viruses have caused great economic losses to the poultry industry. The H9N2 virus is recognized as a donor for internal genes to other AIV subtypes, including the H5N1, H7N9, and H10N8 viruses, which can infect humans, causing a potential threat to public health. The H9N2 virus contains a negative, single-stranded RNA molecule that is susceptible to mutation and reassortment during the replication process, and its surface and internal proteins are divided into distinct lineages [26]. Based on HA, the H9N2 AIVs in Eurasia include the following three lineages: BJ/94-like, G1-like, and Y439/97-like. BJ/94-like and G1-like viruses have become the predominant strains in mainland China since the mid-1990s [37]. However, from 2010–2013, a fittest genotype (G57) containing a PB2 gene from dk/ST/04, which is clustered closely to an H7N7 human isolate, A/Netherlands/219/2003 [26], an M gene from the quail origin qa/HK/G1/97, which was closely related to the emerging H7N9 virus [16, 32], an HA gene from ck/JS/00, and the remaining genes from SH/F/98 emerged with changed antigenicity and improved adaptability in chickens [16]. Currently, the G57 virus is the predominant strain in China since 2013 [16].

In summary, our findings suggest that the H9N2 virus surface glycoproteins have undergone evolution and variation from 2011–2014, which might be related to the G57 virus outbreaks and emergence since 2013. The H9N2 virus internal genes were closely related to those from the human-infected avian influenza viruses H5N1, H7N9, and the emerging influenza virus H10N8. In particular, some NS genes from H9N2 viruses were closely related to the H10N8 and H7N9 viruses, respectively.




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