Rapid evolution of low-pathogenic H9N2 avian influenza viruses following poultry vaccination programmes

Park, Kuk Jin; Kwon, Hyeok‐il; Song, Min‐Suk; Pascua, Philippe Noriel Q.; Baek, Yun Hee; Lee, Jun Han; Jang, Hae-Lan; Lim, Jai-Yun; Mo, In-Pil; Moon, Ho-Jin; Kim, Chul-Joong; Choi, Young Ki

doi:10.1099/vir.0.024992-0

Cited by 96 publications

(73 citation statements)

References 35 publications

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“…Therefore, it is important to investigate whether the circulating H9N2 viruses have undergone further significant genetic and antigenic changes with the advent of vaccination. Antigenic and phylogenetic analysis can also be effective approaches to vaccine development (Park et al 2011;Lee and Song 2013). Therefore, we characterized four H9N2 viruses recently isolated from commercial farms and the vaccine strain both antigenically and phylogenetically.…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran

Bahari

Pourbakhsh

Shoushtari

et al. 2015

Trop Anim Health Prod

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Avian influenza is a highly contagious respiratory disease of poultry caused by influenza A viruses, family Orthomyxoviridae. H9N2 avian influenza outbreaks are a major problem of the poultry industry in Iran. To determine the genetic differences between field viruses and the vaccine strain, the genomes of four strains isolated in 2011 from vaccinated broiler flocks with a history of respiratory illness were sequenced. Genetic and serological comparisons were made. Sequence analysis of the hemagglutinin (HA) and neuraminidase (NA) genes indicated that the isolated strains shared nucleotide homologies of 91.6-93.9 and 90.2-91.7% with the vaccine strain, respectively. Phylogenetic analyses of HA and NA genes showed that all strains isolated in this study fell into the same group and belonged to the influenza A virus (A)/quail/Hong Kong/G1/97 H9N2 sublineage. Several amino acids have changed at the antigenic sites in HA in the field viruses. Extra potential glycosylation sites were observed in the HA and NA proteins expressed by the current isolates relative to those in the vaccine strain. The deduced amino acid sequence at the cleavage site of HA in recent isolates is the KSSR/GLF motif, whereas it is RSSR/GLF in the vaccine strain. A serological analysis revealed that the currently circulating strains are antigenically distinct from the vaccine strain. These results suggest that the commercial vaccine is insufficiently genetically and antigenically similar to the viruses currently circulating in the region. These findings confirm that it is important to monitor the genetic and antigenic variations in H9N2 influenza viruses when selecting a vaccine strain.

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Section: Introductionmentioning

confidence: 99%

Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran

Bahari

Pourbakhsh

Shoushtari

et al. 2015

Trop Anim Health Prod

View full text Add to dashboard Cite

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“…7A). Among the 130 HA sequences obtained in 2009, 38 sequences with 363T, which were genetically close to each other and were all isolated from South Korea, lowered the proportion of HA 363K in 2009 (36). In 1998, H9N2 influenza virus was endemic to China, and the proportion of strains with both PA 672L and HA 363K PA reached its first peak as well (Fig.…”

Section: Figmentioning

confidence: 99%

Molecular Mechanism of the Airborne Transmissibility of H9N2 Avian Influenza A Viruses in Chickens

Zhong

Wang

et al. 2014

J Virol

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H9N2 avian influenza virus has been prevalent in poultry in many parts of the world since the 1990s and occasionally crosses the host barrier, transmitting to mammals, including humans. In recent years, these viruses have contributed genes to H5N1 and H7N9 influenza viruses, threatening public health. To explore the molecular mechanism for the airborne transmission of H9N2 virus, we compared two genetically close strains isolated from chickens in 2001, A/chicken/Shanghai/7/2001(SH7) and A/chicken/Shanghai/14/2001 (SH14). SH7 is airborne transmissible between chickens, whereas SH14 is not. We used reverse genetics and gene swapping to derive recombinant SH7 (rSH7), rSH14, and a panel of reassortant viruses. Among the reassortant viruses, we identified segments HA and PA as governing the airborne transmission among chickens. In addition, the NP and NS genes also contributed to a lesser extent. Furthermore, the mutational analyses showed the transmissibility phenotype predominantly mapped to the HA and PA genes, with HA-K363 and PA-L672 being important for airborne transmissibility among chickens. In addition, the viral infectivity and acid stability are related to the airborne transmissibility. Importantly, airborne transmission studies of 18 arbitrarily chosen H9N2 viruses from our collections confirmed the importance of both 363K in HA and 672L in PA in determining their levels of transmissibility. Our finding elucidates the genetic contributions to H9N2 transmissibility in chickens and highlights the importance of their prevalence in poultry. IMPORTANCEOur study investigates the airborne transmissibility of H9N2 viruses in chickens and the subsequent epidemic. H9N2 virus is the donor for several prevalent reassortant influenza viruses, such as H7N9/2013 and the H5N1 viruses. Poultry as the reservoir hosts of influenza virus is closely associated with human society. Airborne transmission is an efficient pathway for influenza virus transmission among flocks and individuals. Exploring the mechanism of the airborne transmission of the H9N2 virus in chickens could provide essential data regarding prevention and control of influenza endemics and pandemics.

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“…Besides contributing its internal genes to H5N1 and H7N9 viruses, H9N2 virus has been in active genetic exchange with H3N2 and H7N3 viruses (12,33,34). Recent studies demonstrate that H9N2 virus can also easily reassort with the 2009 pandemic H1N1 virus, creating reassortant viruses with higher pathogenicity or better aerosol transmissibility than the parental viruses in mammalian models (35)(36)(37).…”

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confidence: 99%

“…With the massive vaccination against H9N2 infection in poultry in many countries, novel antigenic groups have emerged (34,(43)(44)(45). There is no doubt that a continuous and close surveillance on the antigenic evolution of H9N2 virus will facilitate better strategies for the control of H9N2 virus infection.…”

mentioning

confidence: 99%

Antigenic Mapping of the Hemagglutinin of an H9N2 Avian Influenza Virus Reveals Novel Critical Amino Acid Positions in Antigenic Sites

Wan

et al. 2014

J Virol

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H9N2 influenza virus is undergoing extensive genetic and antigenic evolution, warranting detailed antigenic mapping of its hemagglutinin (HA). Through examining antibody escape mutants of an Asian avian H9N2 virus, we identified 9 critical amino acid positions in H9 antigenic sites. Five of these positions, 164, 167, 168, 196, and 207, have not been reported previously and, thus, represent novel molecular markers for monitoring the antigenic change of H9N2 virus. H9N2 influenza virus is circulating in poultry worldwide. H9N2 virus infection is usually mild in nature but may lead to higher mortality if it is associated with secondary infection (1, 2). In Asia, since its introduction into land-based poultry in the late 1980s, H9N2 virus has been spreading to various avian and mammalian species, including pigs (3, 4). Due to the Q226L mutation (change of Gln to Leu at position 226) in the hemagglutinin (HA) (5-7), a significant proportion of H9N2 isolates have acquired human virus-like receptor specificity (5,8). Consistent with this receptor specificity change, multiple human cases of H9N2 virus infection have been reported (9-12). Moreover, H9N2 virus has provided internal genes for the highly pathogenic H5N1 (9, 13, 14) and novel H7N9 (15) viruses. These have put H9N2 virus high on the list of influenza viruses with pandemic potential.Although the crystal structure of H9 has been solved (16), no details for H9 antigenic epitopes have been elucidated. Previous investigations by other groups have identified multiple amino acids in H9 antigenic sites (17, 18). These are nevertheless far from being sufficient for understanding the H9 antigenic structure. To identify more amino acids constituting H9 antigenic sites, we performed an antigenic mapping of the HA of an avian H9N2 virus A/Chicken/Jiangsu/X1/2004 (hereinafter called X1) (GenBank nucleotide sequence accession number KF688983) with monoclonal antibodies (MAbs).H9-specific MAbs were generated through the fusion of myeloma Sp2/0 cells with splenocytes from a BALB/c mouse immunized with X1 virus (19). The immunization included 3 intraperitoneal inoculations at 2-week intervals and a final boost with live X1 virus (on day 3 before the fusion). Hybridomas were screened by indirect immunofluorescence assay using chicken embryo fibroblast cells infected with X1 virus as the antigen, followed by screening with a hemagglutination inhibition (HI) assay using 4 hemagglutination units of X1 virus (20). Ascitic fluid of each selected hybridoma was generated in mice and used directly (e.g., without further purification or treatment with receptor-destroying enzyme) in the characterization of each MAb. All animal experiments were done in accordance with the institutional animal care guidelines, and the protocol (number 06R015) was approved by the Animal Care Committee at Yangzhou University. A microneutralization (MN) assay was performed in Madin-Darby canine kidney (MDCK) cells, following a previous protocol (21), except that 100 median tissue infectious doses (TCID 50 ) o...

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Rapid evolution of low-pathogenic H9N2 avian influenza viruses following poultry vaccination programmes

Cited by 96 publications

References 35 publications

Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran

Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran

Molecular Mechanism of the Airborne Transmissibility of H9N2 Avian Influenza A Viruses in Chickens

Antigenic Mapping of the Hemagglutinin of an H9N2 Avian Influenza Virus Reveals Novel Critical Amino Acid Positions in Antigenic Sites

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