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Jinhua Liu
Key Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, 100193, Beijing, China

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Journal article
Published: 06 June 2021 in Virology
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Reassortant Eurasian avian-like (EA) H1N1 virus, possessing 2009 pandemic (pdm/09) and triple-reassortant (TR)-derived internal genes, namely G4 genotype, has replaced the G1 genotype EA H1N1 virus (all the genes were of EA origin) and become predominant in swine populations in China. Understanding the pathogenicity of G4 viruses in pigs is of great importance for disease control. Here, we conducted comprehensive analyses of replication and pathogenicity of G4 and G1 EA H1N1 viruses in pigs. G4 virus exhibited enhanced replication, increased duration of virus shedding, and caused more severe respiratory lesions in pigs compared with G1 virus. G4 virus, with viral ribonucleoprotein (vRNP) complex genes of pdm/09 origin, exhibited higher levels of nuclear accumulation and higher polymerase activity, which is essential for improved replication of G4 virus. These findings indicate that G4 virus poses a great threat to both swine industry and public health, and control measures should be urgently implemented.

ACS Style

Haoran Sun; Jiyu Liu; Yihong Xiao; Yuhong Duan; Jizhe Yang; Yu Chen; Yinghui Yu; Han Li; Yuzhong Zhao; Juan Pu; Yipeng Sun; Jinhua Liu; Honglei Sun. Pathogenicity of novel reassortant Eurasian avian-like H1N1 influenza virus in pigs. Virology 2021, 561, 28 -35.

AMA Style

Haoran Sun, Jiyu Liu, Yihong Xiao, Yuhong Duan, Jizhe Yang, Yu Chen, Yinghui Yu, Han Li, Yuzhong Zhao, Juan Pu, Yipeng Sun, Jinhua Liu, Honglei Sun. Pathogenicity of novel reassortant Eurasian avian-like H1N1 influenza virus in pigs. Virology. 2021; 561 ():28-35.

Chicago/Turabian Style

Haoran Sun; Jiyu Liu; Yihong Xiao; Yuhong Duan; Jizhe Yang; Yu Chen; Yinghui Yu; Han Li; Yuzhong Zhao; Juan Pu; Yipeng Sun; Jinhua Liu; Honglei Sun. 2021. "Pathogenicity of novel reassortant Eurasian avian-like H1N1 influenza virus in pigs." Virology 561, no. : 28-35.

Journal article
Published: 17 March 2021 in Journal of Virology
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H9N2 avian influenza virus (AIV) is regarded as a principal donor of viral genes through reassortment to cocirculating influenza viruses that can result in zoonotic reassortants. Whether H9N2 virus can maintain a sustained evolutionary impact on such reassortants is unclear. Since 2013, avian H7N9 virus had caused five sequential human epidemics in China; the fifth wave in 2016 to 2017 was by far the largest, but the mechanistic explanation behind the scale of infection is not clear. Here, we found that just prior to the fifth H7N9 virus epidemic, H9N2 viruses had phylogenetically mutated into new subclades, changed antigenicity, and increased their prevalence in chickens vaccinated with existing H9N2 vaccines. In turn, the new H9N2 virus subclades of PB2 and PA genes, housing mammalian adaptive mutations, were reassorted into cocirculating H7N9 virus to create a novel dominant H7N9 virus genotype that was responsible for the fifth H7N9 virus epidemic. H9N2-derived PB2 and PA genes in H7N9 virus conferred enhanced polymerase activity in human cells at 33°C and 37°C and increased viral replication in the upper and lower respiratory tracts of infected mice, which could account for the sharp increase in human cases of H7N9 virus infection in the 2016–2017 epidemic. The role of H9N2 virus in the continual mutation of H7N9 virus highlights the public health significance of H9N2 virus in the generation of variant reassortants of increasing zoonotic potential. IMPORTANCE Avian H9N2 influenza virus, although primarily restricted to chicken populations, is a major threat to human public health by acting as a donor of variant viral genes through reassortment to cocirculating influenza viruses. We established that the high prevalence of evolving H9N2 virus in vaccinated flocks played a key role as a donor of new subclade PB2 and PA genes in the generation of a dominant H7N9 virus genotype (genotype 72 [G72]) with enhanced infectivity in humans during the 2016–2017 H7N9 virus epidemic. Our findings emphasize that the ongoing evolution of prevalent H9N2 virus in chickens is an important source, via reassortment, of mammalian adaptive genes for other influenza virus subtypes. Thus, close monitoring of the prevalence and variants of H9N2 virus in chicken flocks is necessary for the detection of zoonotic mutations.

ACS Style

Juan Pu; Yanbo Yin; Jiyu Liu; Xinyu Wang; Yong Zhou; Zejiang Wang; Yipeng Sun; Honglei Sun; Fangtao Li; Jingwei Song; Runkang Qu; Weihua Gao; Dongdong Wang; Zhen Wang; Shijie Yan; Mingyue Chen; Jinfeng Zeng; Zhimin Jiang; Haoran Sun; Yanan Zong; Chenxi Wang; Qi Tong; Yuhai Bi; Yinhua Huang; Xiangjun Du; Kin-Chow Chang; Jinhua Liu. Reassortment with Dominant Chicken H9N2 Influenza Virus Contributed to the Fifth H7N9 Virus Human Epidemic. Journal of Virology 2021, 95, 1 .

AMA Style

Juan Pu, Yanbo Yin, Jiyu Liu, Xinyu Wang, Yong Zhou, Zejiang Wang, Yipeng Sun, Honglei Sun, Fangtao Li, Jingwei Song, Runkang Qu, Weihua Gao, Dongdong Wang, Zhen Wang, Shijie Yan, Mingyue Chen, Jinfeng Zeng, Zhimin Jiang, Haoran Sun, Yanan Zong, Chenxi Wang, Qi Tong, Yuhai Bi, Yinhua Huang, Xiangjun Du, Kin-Chow Chang, Jinhua Liu. Reassortment with Dominant Chicken H9N2 Influenza Virus Contributed to the Fifth H7N9 Virus Human Epidemic. Journal of Virology. 2021; 95 (11):1.

Chicago/Turabian Style

Juan Pu; Yanbo Yin; Jiyu Liu; Xinyu Wang; Yong Zhou; Zejiang Wang; Yipeng Sun; Honglei Sun; Fangtao Li; Jingwei Song; Runkang Qu; Weihua Gao; Dongdong Wang; Zhen Wang; Shijie Yan; Mingyue Chen; Jinfeng Zeng; Zhimin Jiang; Haoran Sun; Yanan Zong; Chenxi Wang; Qi Tong; Yuhai Bi; Yinhua Huang; Xiangjun Du; Kin-Chow Chang; Jinhua Liu. 2021. "Reassortment with Dominant Chicken H9N2 Influenza Virus Contributed to the Fifth H7N9 Virus Human Epidemic." Journal of Virology 95, no. 11: 1.

Journal article
Published: 12 March 2021 in Veterinary Microbiology
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The H1N1 influenza virus of swine-origin was responsible for the H1N1 pandemic in 2009 (pdm/09 H1N1), where the virus was transmitted to humans and then spread between people, and its continued circulation has resulted in it becoming a seasonal human flu virus. Since 2016, the matrix (M) gene of pdm/09 H1N1 has been involved in the reassortment of swine influenza viruses (SIVs) in China and has gradually become a dominant genotype in pigs. However, whether M gene substitution will influence the fitness of emerging SIVs remains unclear. Here, we analyzed the biological characteristics of SIVs with the M gene from Eurasian avian-like (EA) SIV or pdm/09 H1N1 in mammals and found that SIVs containing the pdm/09-M gene exhibit stronger virulence in mice, more efficient respiratory droplet transmission between ferrets, and increased transcription of viral genes in A549 cells compared with those containing EA-M. We also determined the functional significance of the pdm/09-M gene in conferring an elevated release of progeny viruses comprised of largely filamentous virions rather than spherical virions. Our study suggests that pdm/09-M plays a crucial role in the genesis of emerging SIVs in terms of the potential prevalence in the population.

ACS Style

Junda Zhu; Zhimin Jiang; Jinhua Liu. The matrix gene of pdm/09 H1N1 contributes to the pathogenicity and transmissibility of SIV in mammals. Veterinary Microbiology 2021, 255, 109039 .

AMA Style

Junda Zhu, Zhimin Jiang, Jinhua Liu. The matrix gene of pdm/09 H1N1 contributes to the pathogenicity and transmissibility of SIV in mammals. Veterinary Microbiology. 2021; 255 ():109039.

Chicago/Turabian Style

Junda Zhu; Zhimin Jiang; Jinhua Liu. 2021. "The matrix gene of pdm/09 H1N1 contributes to the pathogenicity and transmissibility of SIV in mammals." Veterinary Microbiology 255, no. : 109039.

Journal article
Published: 10 March 2021 in Journal of Virology
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Infection of the CNS is a serious complication of human cases of AIV infection. The viral and host factors associated with neurovirulence of AIV infection are not well understood.

ACS Style

Xuxiao Zhang; Juan Pu; Yipeng Sun; Yuhai Bi; Zhimin Jiang; GuanLong Xu; Hongyu Zhang; Jing Cao; Kin-Chow Chang; Jinhua Liu; Honglei Sun. Neurovirulence of Avian Influenza Virus Is Dependent on the Interaction of Viral NP Protein with FMRP in the Murine Brain. Journal of Virology 2021, 95, 1 .

AMA Style

Xuxiao Zhang, Juan Pu, Yipeng Sun, Yuhai Bi, Zhimin Jiang, GuanLong Xu, Hongyu Zhang, Jing Cao, Kin-Chow Chang, Jinhua Liu, Honglei Sun. Neurovirulence of Avian Influenza Virus Is Dependent on the Interaction of Viral NP Protein with FMRP in the Murine Brain. Journal of Virology. 2021; 95 (7):1.

Chicago/Turabian Style

Xuxiao Zhang; Juan Pu; Yipeng Sun; Yuhai Bi; Zhimin Jiang; GuanLong Xu; Hongyu Zhang; Jing Cao; Kin-Chow Chang; Jinhua Liu; Honglei Sun. 2021. "Neurovirulence of Avian Influenza Virus Is Dependent on the Interaction of Viral NP Protein with FMRP in the Murine Brain." Journal of Virology 95, no. 7: 1.

Journal article
Published: 03 February 2021 in Viruses
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The long-term control strategy of SARS-CoV-2 and other major respiratory viruses needs to include antivirals to treat acute infections, in addition to the judicious use of effective vaccines. Whilst COVID-19 vaccines are being rolled out for mass vaccination, the modest number of antivirals in use or development for any disease bears testament to the challenges of antiviral development. We recently showed that non-cytotoxic levels of thapsigargin (TG), an inhibitor of the sarcoplasmic/endoplasmic reticulum (ER) Ca2+ ATPase pump, induces a potent host innate immune antiviral response that blocks influenza A virus replication. Here we show that TG is also highly effective in blocking the replication of respiratory syncytial virus (RSV), common cold coronavirus OC43, SARS-CoV-2 and influenza A virus in immortalized or primary human cells. TG’s antiviral performance was significantly better than remdesivir and ribavirin in their respective inhibition of OC43 and RSV. Notably, TG was just as inhibitory to coronaviruses (OC43 and SARS-CoV-2) and influenza viruses (USSR H1N1 and pdm 2009 H1N1) in separate infections as in co-infections. Post-infection oral gavage of acid-stable TG protected mice against a lethal influenza virus challenge. Together with its ability to inhibit the different viruses before or during active infection, and with an antiviral duration of at least 48 h post-TG exposure, we propose that TG (or its derivatives) is a promising broad-spectrum inhibitor against SARS-CoV-2, OC43, RSV and influenza virus.

ACS Style

Sarah Al-Beltagi; Cristian Preda; Leah Goulding; Joe James; Juan Pu; Paul Skinner; Zhimin Jiang; Belinda Wang; Jiayun Yang; Ashley Banyard; Kenneth Mellits; Pavel Gershkovich; Christopher Hayes; Jonathan Nguyen-Van-Tam; Ian Brown; Jinhua Liu; Kin-Chow Chang. Thapsigargin Is a Broad-Spectrum Inhibitor of Major Human Respiratory Viruses: Coronavirus, Respiratory Syncytial Virus and Influenza A Virus. Viruses 2021, 13, 234 .

AMA Style

Sarah Al-Beltagi, Cristian Preda, Leah Goulding, Joe James, Juan Pu, Paul Skinner, Zhimin Jiang, Belinda Wang, Jiayun Yang, Ashley Banyard, Kenneth Mellits, Pavel Gershkovich, Christopher Hayes, Jonathan Nguyen-Van-Tam, Ian Brown, Jinhua Liu, Kin-Chow Chang. Thapsigargin Is a Broad-Spectrum Inhibitor of Major Human Respiratory Viruses: Coronavirus, Respiratory Syncytial Virus and Influenza A Virus. Viruses. 2021; 13 (2):234.

Chicago/Turabian Style

Sarah Al-Beltagi; Cristian Preda; Leah Goulding; Joe James; Juan Pu; Paul Skinner; Zhimin Jiang; Belinda Wang; Jiayun Yang; Ashley Banyard; Kenneth Mellits; Pavel Gershkovich; Christopher Hayes; Jonathan Nguyen-Van-Tam; Ian Brown; Jinhua Liu; Kin-Chow Chang. 2021. "Thapsigargin Is a Broad-Spectrum Inhibitor of Major Human Respiratory Viruses: Coronavirus, Respiratory Syncytial Virus and Influenza A Virus." Viruses 13, no. 2: 234.

Research article
Published: 01 January 2021 in Emerging Microbes & Infections
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Pandemic influenza, typically caused by the reassortment of human and avian influenza viruses, can result in severe or fatal infections in humans. Timely identification of potential pandemic viruses must be a priority in influenza virus surveillance. However, the range of host species responsible for the generation of novel pandemic influenza viruses remains unclear. In this study, we conducted serological surveys for avian and human influenza virus infections in farmed mink and determined the susceptibility of mink to prevailing avian and human virus subtypes. The results showed that farmed mink were commonly infected with human (H3N2 and H1N1/pdm) and avian (H7N9, H5N6, and H9N2) influenza A viruses. Correlational analysis indicated that transmission of human influenza viruses occurred from humans to mink, and that feed source was a probable route of avian influenza virus transmission to farmed mink. Animal experiments showed that mink were susceptible and permissive to circulating avian and human influenza viruses, and that human influenza viruses (H3N2 and H1N1/pdm), but not avian viruses, were capable of aerosol transmission among mink. These results indicate that farmed mink could be highly permissive “mixing vessels” for the reassortment of circulating human and avian influenza viruses. Therefore, to reduce the risk of emergence of novel pandemic viruses, feeding mink with raw poultry by-products should not be permitted, and epidemiological surveillance of influenza viruses in mink farms should be urgently implemented.

ACS Style

Honglei Sun; Fangtao Li; Qingzhi Liu; Jianyong Du; Litao Liu; Haoran Sun; Chong Li; Jiyu Liu; Xin Zhang; Jizhe Yang; Yuhong Duan; Yuhai Bi; Juan Pu; Yipeng Sun; Qi Tong; Yongqiang Wang; Xiangjun Du; Yuelong Shu; Kin-Chow Chang; Jinhua Liu. Mink is a highly susceptible host species to circulating human and avian influenza viruses. Emerging Microbes & Infections 2021, 10, 472 -480.

AMA Style

Honglei Sun, Fangtao Li, Qingzhi Liu, Jianyong Du, Litao Liu, Haoran Sun, Chong Li, Jiyu Liu, Xin Zhang, Jizhe Yang, Yuhong Duan, Yuhai Bi, Juan Pu, Yipeng Sun, Qi Tong, Yongqiang Wang, Xiangjun Du, Yuelong Shu, Kin-Chow Chang, Jinhua Liu. Mink is a highly susceptible host species to circulating human and avian influenza viruses. Emerging Microbes & Infections. 2021; 10 (1):472-480.

Chicago/Turabian Style

Honglei Sun; Fangtao Li; Qingzhi Liu; Jianyong Du; Litao Liu; Haoran Sun; Chong Li; Jiyu Liu; Xin Zhang; Jizhe Yang; Yuhong Duan; Yuhai Bi; Juan Pu; Yipeng Sun; Qi Tong; Yongqiang Wang; Xiangjun Du; Yuelong Shu; Kin-Chow Chang; Jinhua Liu. 2021. "Mink is a highly susceptible host species to circulating human and avian influenza viruses." Emerging Microbes & Infections 10, no. 1: 472-480.

Journal article
Published: 09 November 2020 in Journal of Virology
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The host range of an influenza A virus is determined by species-specific interactions between virus and host cell factors. Host miRNAs can regulate influenza A virus replication; however, the role of miRNAs in host species specificity is unclear. Here, we show that the induced expression of ssc-miR-221-3p and ssc-miR-222 in swine cells is modulated by NF-κB P65 phosphorylation in response to AIV infection but not swine influenza virus infection. ssc-miR-221-3p and ssc-miR-222 exerted antiviral function via targeting viral RNAs and causing apoptosis by inhibiting the expression of HMBOX1 in host cells. These findings uncover miRNAs as a host range restriction factor that limits cross-species infection of influenza A virus.

ACS Style

Jingwei Song; Honglei Sun; Haoran Sun; Zhimin Jiang; Junda Zhu; Chenxi Wang; Weihua Gao; Tong Wang; Juan Pu; Yipeng Sun; Hsiang-Yu Yuan; Jinhua Liu. Swine MicroRNAs ssc-miR-221-3p and ssc-miR-222 Restrict the Cross-Species Infection of Avian Influenza Virus. Journal of Virology 2020, 94, 1 .

AMA Style

Jingwei Song, Honglei Sun, Haoran Sun, Zhimin Jiang, Junda Zhu, Chenxi Wang, Weihua Gao, Tong Wang, Juan Pu, Yipeng Sun, Hsiang-Yu Yuan, Jinhua Liu. Swine MicroRNAs ssc-miR-221-3p and ssc-miR-222 Restrict the Cross-Species Infection of Avian Influenza Virus. Journal of Virology. 2020; 94 (23):1.

Chicago/Turabian Style

Jingwei Song; Honglei Sun; Haoran Sun; Zhimin Jiang; Junda Zhu; Chenxi Wang; Weihua Gao; Tong Wang; Juan Pu; Yipeng Sun; Hsiang-Yu Yuan; Jinhua Liu. 2020. "Swine MicroRNAs ssc-miR-221-3p and ssc-miR-222 Restrict the Cross-Species Infection of Avian Influenza Virus." Journal of Virology 94, no. 23: 1.

Journal article
Published: 27 October 2020 in mBio
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The immune system produces antibodies to protect the human body from harmful invaders. The monoclonal antibody (MAb) is one kind of effective antivirals. In this study, we isolated an antibody (Z2B3) from an H7N9 influenza virus-infected child. It shows cross-reactivity to both group 1 (N1) and group 2 (N9) neuraminidases (NAs) but is sensitive to N1 NA with a K432E substitution. Structural analysis of the NA-antibody fragment antigen-binding (Fab) complex provides a clue for antibody modification, and the modified antibody restored binding and inhibition to recently drifted N1 NA and regained protection against the variant influenza strain. This finding suggests that antibodies to NA may be a useful therapy and can be in principle edited to defeat drifted influenza virus.

ACS Style

HaiHai Jiang; Weiyu Peng; Jianxun Qi; Yan Chai; Hao Song; Yuhai Bi; Pramila Rijal; Haiyuan Wang; Babayemi O. Oladejo; Jinhua Liu; Yi Shi; George F. Gao; Alain R. Townsend; Yan Wu. Structure-Based Modification of an Anti-neuraminidase Human Antibody Restores Protection Efficacy against the Drifted Influenza Virus. mBio 2020, 11, 1 .

AMA Style

HaiHai Jiang, Weiyu Peng, Jianxun Qi, Yan Chai, Hao Song, Yuhai Bi, Pramila Rijal, Haiyuan Wang, Babayemi O. Oladejo, Jinhua Liu, Yi Shi, George F. Gao, Alain R. Townsend, Yan Wu. Structure-Based Modification of an Anti-neuraminidase Human Antibody Restores Protection Efficacy against the Drifted Influenza Virus. mBio. 2020; 11 (5):1.

Chicago/Turabian Style

HaiHai Jiang; Weiyu Peng; Jianxun Qi; Yan Chai; Hao Song; Yuhai Bi; Pramila Rijal; Haiyuan Wang; Babayemi O. Oladejo; Jinhua Liu; Yi Shi; George F. Gao; Alain R. Townsend; Yan Wu. 2020. "Structure-Based Modification of an Anti-neuraminidase Human Antibody Restores Protection Efficacy against the Drifted Influenza Virus." mBio 11, no. 5: 1.

Journal article
Published: 27 September 2020 in Viruses
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Influenza A virus is a major global pathogen of humans, and there is an unmet need for effective antivirals. Current antivirals against influenza A virus directly target the virus and are vulnerable to mutational resistance. Harnessing an effective host antiviral response is an attractive alternative. We show that brief exposure to low, non-toxic doses of thapsigargin (TG), an inhibitor of the sarcoplasmic/endoplasmic reticulum (ER) Ca2+ ATPase pump, promptly elicits an extended antiviral state that dramatically blocks influenza A virus production. Crucially, oral administration of TG protected mice against lethal virus infection and reduced virus titres in the lungs of treated mice. TG-induced ER stress unfolded protein response appears as a key driver responsible for activating a spectrum of host antiviral defences that include an enhanced type I/III interferon response. Our findings suggest that TG is potentially a viable host-centric antiviral for the treatment of influenza A virus infection without the inherent problem of drug resistance.

ACS Style

Leah V. Goulding; Jiayun Yang; Zhimin Jiang; Hongyu Zhang; Daniel Lea; Richard D. Emes; Tania Dottorini; Juan Pu; Jinhua Liu; Kin-Chow Chang. Thapsigargin at Non-Cytotoxic Levels Induces a Potent Host Antiviral Response that Blocks Influenza A Virus Replication. Viruses 2020, 12, 1093 .

AMA Style

Leah V. Goulding, Jiayun Yang, Zhimin Jiang, Hongyu Zhang, Daniel Lea, Richard D. Emes, Tania Dottorini, Juan Pu, Jinhua Liu, Kin-Chow Chang. Thapsigargin at Non-Cytotoxic Levels Induces a Potent Host Antiviral Response that Blocks Influenza A Virus Replication. Viruses. 2020; 12 (10):1093.

Chicago/Turabian Style

Leah V. Goulding; Jiayun Yang; Zhimin Jiang; Hongyu Zhang; Daniel Lea; Richard D. Emes; Tania Dottorini; Juan Pu; Jinhua Liu; Kin-Chow Chang. 2020. "Thapsigargin at Non-Cytotoxic Levels Induces a Potent Host Antiviral Response that Blocks Influenza A Virus Replication." Viruses 12, no. 10: 1093.

Review
Published: 07 August 2020 in Viruses
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Avian influenza A viruses (AIVs), as a zoonotic agent, dramatically impacts public health and the poultry industry. Although low pathogenic avian influenza virus (LPAIV) incidence and mortality are relatively low, the infected hosts can act as a virus carrier and provide a resource pool for reassortant influenza viruses. At present, vaccination is the most effective way to eradicate AIVs from commercial poultry. The inactivated vaccines can only stimulate humoral immunity, rather than cellular and mucosal immune responses, while failing to effectively inhibit the replication and spread of AIVs in the flock. In recent years, significant progresses have been made in the understanding of the mechanisms underlying the vaccine antigen activities at the mucosal surfaces and the development of safe and efficacious mucosal vaccines that mimic the natural infection route and cut off the AIVs infection route. Here, we discussed the current status and advancement on mucosal immunity, the means of establishing mucosal immunity, and finally a perspective for design of AIVs mucosal vaccines. Hopefully, this review will help to not only understand and predict AIVs infection characteristics in birds but also extrapolate them for distinction or applicability in mammals, including humans.

ACS Style

Tong Wang; Fanhua Wei; Jinhua Liu. Emerging Role of Mucosal Vaccine in Preventing Infection with Avian Influenza A Viruses. Viruses 2020, 12, 862 .

AMA Style

Tong Wang, Fanhua Wei, Jinhua Liu. Emerging Role of Mucosal Vaccine in Preventing Infection with Avian Influenza A Viruses. Viruses. 2020; 12 (8):862.

Chicago/Turabian Style

Tong Wang; Fanhua Wei; Jinhua Liu. 2020. "Emerging Role of Mucosal Vaccine in Preventing Infection with Avian Influenza A Viruses." Viruses 12, no. 8: 862.

Short report
Published: 12 November 2019 in Virology Journal
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Background H9N2 influenza viruses continuously circulate in multiple avian species and are repeatedly transmitted to humans, posing a significant threat to public health. To investigate the adaptation ability of H9N2 avian influenza viruses (AIVs) to mammals and the mutations related to the host switch events, we serially passaged in mice two H9N2 viruses of different HA lineages — A/Quail/Hong Kong/G1/97 (G1) of the G1-like lineage and A/chicken/Shandong/ZB/2007 (ZB) of the BJ/94-like lineage —and generated two mouse-adapted H9N2 viruses (G1-MA and ZB-MA) that possessed significantly higher virulence than the wide-type viruses. Finding ZB-MA replicated systemically in mice. Genomic sequence alignment revealed 10 amino acid mutations coded by 4 different gene segments (PB2, PA, HA, and M) in G1-MA compared with the G1 virus and 23 amino acid mutations in 5 gene segments (PB1, PA, HA, M, and NS) in ZB-MA compared to ZB virus, indicating that the mutations in the polymerase, HA, M, and NS genes play critical roles in the adaptation of H9N2 AIVs to mammals, especially, the mutations of M1-Q198H and M1-A239T were shared in G1-MA and ZB-MA viruses. Additionally, several substitutions showed a higher frequency in human influenza viruses compared with avian viruses. Conclusions Different lineages of H9N2 could adapt well in mice and some viruses could gain the ability to replicate systemically and become neurovirulent. Thus, it is essential to pay attention to the mammalian adaptive evolution of the H9N2 virus.

ACS Style

Zhe Hu; Yiran Zhang; Zhen Wang; Jingjing Wang; Qi Tong; Mingyang Wang; Honglei Sun; Juan Pu; Changqing Liu; Jinhua Liu; Yipeng Sun. Mouse-adapted H9N2 avian influenza virus causes systemic infection in mice. Virology Journal 2019, 16, 135 -8.

AMA Style

Zhe Hu, Yiran Zhang, Zhen Wang, Jingjing Wang, Qi Tong, Mingyang Wang, Honglei Sun, Juan Pu, Changqing Liu, Jinhua Liu, Yipeng Sun. Mouse-adapted H9N2 avian influenza virus causes systemic infection in mice. Virology Journal. 2019; 16 (1):135-8.

Chicago/Turabian Style

Zhe Hu; Yiran Zhang; Zhen Wang; Jingjing Wang; Qi Tong; Mingyang Wang; Honglei Sun; Juan Pu; Changqing Liu; Jinhua Liu; Yipeng Sun. 2019. "Mouse-adapted H9N2 avian influenza virus causes systemic infection in mice." Virology Journal 16, no. 1: 135-8.

Case report
Published: 11 April 2019 in BMC Veterinary Research
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In May 2017, 17 dogs in a German Shepherd breeding kennel in northern China developed respiratory clinical signs. The owner treated the dogs with an intravenous injection of Shuang-Huang-lian, a traditional Chinese medicine, and azithromycin. The respiratory signs improved 3 days post-treatment, however, cysts were observed in the necks of eight dogs, and three of them died in the following 2 days. Quantitative real-time PCR was used to detect canine influenza virus (CIV). All of the dogs in this kennel were positive and the remaining 14 dogs had seroconverted. Two of the dogs were taken to the China Agricultural University Veterinary Teaching Hospital for further examination. Two strains of influenza virus (A/canine/Beijing/0512-133/2017 and A/canine/Beijing/0512-137/2017) isolated from the nasal swabs of these dogs were sequenced and identified as avian-origin H3N2 CIV. For the two dogs admitted to the hospital, hematology showed mild inflammation and radiograph results indicated pneumonia. Cyst fluid was plated for bacterial culture and bacterial 16 s rRNA gene PCR was performed, followed by Sanger sequencing. The results indicated an Enterococcus faecalis infection. Antimicrobial susceptibility tests were performed and dogs were treated with enrofloxacin. All 14 remaining dogs recovered within 16 days. Coinfection of H3N2 CIV and Enterococcus faecalis was detected in dogs, which has not been reported previously. Our results highlight that CIV infection might promote the secondary infection of opportunistic bacteria and cause more severe and complicated clinical outcomes.

ACS Style

Liwei Zhou; Haoran Sun; Shikai Song; Jinhua Liu; Zhaofei Xia; Yipeng Sun; Yanli Lyu. H3N2 canine influenza virus and Enterococcus faecalis coinfection in dogs in China. BMC Veterinary Research 2019, 15, 113 .

AMA Style

Liwei Zhou, Haoran Sun, Shikai Song, Jinhua Liu, Zhaofei Xia, Yipeng Sun, Yanli Lyu. H3N2 canine influenza virus and Enterococcus faecalis coinfection in dogs in China. BMC Veterinary Research. 2019; 15 (1):113.

Chicago/Turabian Style

Liwei Zhou; Haoran Sun; Shikai Song; Jinhua Liu; Zhaofei Xia; Yipeng Sun; Yanli Lyu. 2019. "H3N2 canine influenza virus and Enterococcus faecalis coinfection in dogs in China." BMC Veterinary Research 15, no. 1: 113.

Journal article
Published: 11 January 2019 in BMC Genomics
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Long non-coding RNAs (lncRNAs) are important component of mammalian genomes, where their numbers are even larger than that of protein-coding genes. For example, human (Homo sapiens) (96,308 vs. 20,376) and mouse (Mus musculus) (87,774 vs. 22,630) have more lncRNA genes than protein-coding genes in the NONCODEv5 database. Recently, mammalian lncRNAs were reported to play critical roles in immune response to influenza A virus infections. Such observation inspired us to identify lncRNAs related to immune response to influenza A virus in duck, which is the most important natural host of influenza A viruses. We explored features of 62,447 lncRNAs from human, mouse, chicken, zebrafish and elegans, and developed a pipeline to identify lncRNAs using the identified features with transcriptomic data. We then collected 151,970 assembled transcripts from RNA-Seq data of 21 individuals from three tissues and annotated 4094 duck lncRNAs. Comparing to duck protein-coding transcripts, we found that 4094 lncRNAs had smaller number of exons (2.4 vs. 10.2) and longer length of transcripts (1903.0 bp vs. 1686.9 bp) on average. Among them, 3586 (87.6%) lncRNAs located in intergenic regions and 619 lncRNAs showed differential expression in ducks infected by H5N1 virus when compared to control individuals. 58 lncRNAs were involved into two co-expressional modules related to anti-influenza A virus immune response. Moreover, we confirmed that eight lncRNAs showed remarkably differential expression both in vivo (duck individuals) and in vitro (duck embryo fibroblast cells, DEF cells) after infected with H5N1 viruses, implying they might play important roles in response to influenza A virus infection. This study presented an example to annotate lncRNA in new species based on model species using transcriptome data. These data and analysis provide information for duck lncRNAs’ function in immune response to influenza A virus.

ACS Style

Chang Lu; Yanling Xing; Han Cai; Yirong Shi; Jinhua Liu; Yinhua Huang. Identification and analysis of long non-coding RNAs in response to H5N1 influenza viruses in duck (Anas platyrhynchos). BMC Genomics 2019, 20, 36 .

AMA Style

Chang Lu, Yanling Xing, Han Cai, Yirong Shi, Jinhua Liu, Yinhua Huang. Identification and analysis of long non-coding RNAs in response to H5N1 influenza viruses in duck (Anas platyrhynchos). BMC Genomics. 2019; 20 (1):36.

Chicago/Turabian Style

Chang Lu; Yanling Xing; Han Cai; Yirong Shi; Jinhua Liu; Yinhua Huang. 2019. "Identification and analysis of long non-coding RNAs in response to H5N1 influenza viruses in duck (Anas platyrhynchos)." BMC Genomics 20, no. 1: 36.

Journal article
Published: 04 January 2019 in Virology
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H9N2 avian influenza viruses (AIVs) were prevailing in chickens, causing great economic losses and public health threats. In this study, turkey herpesviruses (HVT) was cloned as an infectious bacterial artificial chromosomes (BAC). Recombinant HVT (rHVT-H9) containing hemagglutinin (HA) gene from H9N2 virus were constructed via galactokinase (galK) selection and clustered regularly interspaced short palindromic repeats/associated 9 (CRISPR/Cas9) gene editing system. The recombinant rHVT-H9 showed no difference with parent HVT in plague morphology and virus replication kinetics. H9 protein expression of rHVT-H9 could be detected by western blot and indirect immunofluorescence assay (IFA) in vitro and in vivo. Immunization with rHVT-H9 could induce robust humoral and cellular immunity in chickens. In the challenge study, no chicken shed H9N2 virus from oropharynx and cloaca, and no H9N2 virus was found in viscera in vaccination groups. The result suggests that rHVT-H9 provides effective protection against H9N2 AIV in chickens.

ACS Style

Litao Liu; Tong Wang; Mingyang Wang; Qi Tong; Yipeng Sun; Juan Pu; Honglei Sun; Jinhua Liu. Recombinant turkey herpesvirus expressing H9 hemagglutinin providing protection against H9N2 avian influenza. Virology 2019, 529, 7 -15.

AMA Style

Litao Liu, Tong Wang, Mingyang Wang, Qi Tong, Yipeng Sun, Juan Pu, Honglei Sun, Jinhua Liu. Recombinant turkey herpesvirus expressing H9 hemagglutinin providing protection against H9N2 avian influenza. Virology. 2019; 529 ():7-15.

Chicago/Turabian Style

Litao Liu; Tong Wang; Mingyang Wang; Qi Tong; Yipeng Sun; Juan Pu; Honglei Sun; Jinhua Liu. 2019. "Recombinant turkey herpesvirus expressing H9 hemagglutinin providing protection against H9N2 avian influenza." Virology 529, no. : 7-15.

Journal article
Published: 21 May 2018 in Veterinary Microbiology
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The most commonly utilized inactivated influenza vaccines (IIVs) are usually deficient in cross immunity against divergent viruses. On the other hand, live attenuated influenza vaccines (LAIVs) are proved to be more effective in cross-protective immunity. We previously developed a H9N2 LAIV and verified its effective protection against a broad spectrum of H9N2 strains. In the present study, we evaluated its cross-immunity against H5N2 virus, a representative subtype of currently predominant H5 highly pathogenic avian influenza viruses. All chickens vaccinated with this LAIV survived from challenge of H5N2 virus in a lethal dose, and viral proliferation was effectively inhibited, as well as pathological lesions. Vaccination of this LAIV significantly activated H5N2-reactive CD4+ and CD8+ T cells in lungs. These LAIV-activated cross-reactive T cells expanded robustly following H5N2 exposure, and the increasing tendency was temporally correlated with viral clearance. Besides cellular immunity, factors of humoral immunity also play a contributing role in cross-immunity. Passively transferring H9N2 LAIV anti-serum resulted in 100% survival rate to chickens against H5N2 virus. Within components of the anti-serum, cross-binding IgGs against nucleoprotein (NP) of H5N2 virus were found of a contributing role in the cross immunity. These results indicate that this H9N2 LAIV represents a promising strategy for controlling highly pathogenic H5N2 virus in chickens. The cross immunity was partly attributed to LAIV activated H5N2-cross-reactive T cells and partly attributed to cross-binding IgGs against NP.

ACS Style

Mingyang Wang; YanDi Wei; Juan Pu; GuoXia Bing; Yipeng Sun; Honglei Sun; Fanhua Wei; Jinhua Liu. Cross- immunity of a H9N2 live attenuated influenza vaccine against H5N2 highly pathogenic avian influenza virus in chickens. Veterinary Microbiology 2018, 220, 57 -66.

AMA Style

Mingyang Wang, YanDi Wei, Juan Pu, GuoXia Bing, Yipeng Sun, Honglei Sun, Fanhua Wei, Jinhua Liu. Cross- immunity of a H9N2 live attenuated influenza vaccine against H5N2 highly pathogenic avian influenza virus in chickens. Veterinary Microbiology. 2018; 220 ():57-66.

Chicago/Turabian Style

Mingyang Wang; YanDi Wei; Juan Pu; GuoXia Bing; Yipeng Sun; Honglei Sun; Fanhua Wei; Jinhua Liu. 2018. "Cross- immunity of a H9N2 live attenuated influenza vaccine against H5N2 highly pathogenic avian influenza virus in chickens." Veterinary Microbiology 220, no. : 57-66.

Journal article
Published: 01 August 2017 in Virology
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Previous studies have identified a functional role of PA-X for influenza viruses in mice and avian species; however, its role in swine remains unknown. Toward this, we constructed PA-X deficient virus (Sw-FS) in the background of a Triple-reassortment (TR) H1N2 swine influenza virus (SIV) to assess the impact of PA-X in viral virulence in pigs. Expression of PA-X in TR H1N2 SIV enhanced viral replication and host protein synthesis shutoff, and inhibited the mRNA levels of type I IFNs and proinflammatory cytokines in porcine cells. A delay of proinflammatory responses was observed in lungs of pigs infected by wild type SIV (Sw-WT) compared to Sw-FS. Furthermore, Sw-WT virus replicated and transmitted more efficiently than Sw-FS in pigs. These results highlight the importance of PA-X in the moderation of virulence and immune responses of TR SIV in swine, which indicated that PA-X is a pro-virulence factor in TR SIV in pigs.

ACS Style

GuanLong Xu; Xuxiao Zhang; Qinfang Liu; GuoXia Bing; Zhe Hu; Honglei Sun; Xin Xiong; Ming Jiang; Qiming He; Yu Wang; Juan Pu; Xin Guo; Hanchun Yang; Jinhua Liu; Yipeng Sun. PA-X protein contributes to virulence of triple-reassortant H1N2 influenza virus by suppressing early immune responses in swine. Virology 2017, 508, 45 -53.

AMA Style

GuanLong Xu, Xuxiao Zhang, Qinfang Liu, GuoXia Bing, Zhe Hu, Honglei Sun, Xin Xiong, Ming Jiang, Qiming He, Yu Wang, Juan Pu, Xin Guo, Hanchun Yang, Jinhua Liu, Yipeng Sun. PA-X protein contributes to virulence of triple-reassortant H1N2 influenza virus by suppressing early immune responses in swine. Virology. 2017; 508 ():45-53.

Chicago/Turabian Style

GuanLong Xu; Xuxiao Zhang; Qinfang Liu; GuoXia Bing; Zhe Hu; Honglei Sun; Xin Xiong; Ming Jiang; Qiming He; Yu Wang; Juan Pu; Xin Guo; Hanchun Yang; Jinhua Liu; Yipeng Sun. 2017. "PA-X protein contributes to virulence of triple-reassortant H1N2 influenza virus by suppressing early immune responses in swine." Virology 508, no. : 45-53.

Journal article
Published: 01 July 2017 in Antiviral Research
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Influenza virus infection is a global public health issue. The efficacy of antiviral agents for influenza virus has been limited by the emergence of drug-resistant virus strains. Thus, there is an urgent need to identify novel antiviral therapies. Our previous studies have found that Cryptoporus volvatus extract can potently inhibit influenza virus replication in vitro and in vivo. However, the effective component of Cryptoporus volvatus, which mediates the antiviral activity, hasn't been identified. Here, we identified a novel anti-influenza virus molecule, Cryptoporic acid E (CAE), from Cryptoporus volvatus. Our results showed that CAE had broad-spectrum anti-influenza activity against 2009 pandemic strain A/Beijing/07/2009 (H1N1/09pdm), seasonal strain A/Beijing/CAS0001/2007(H3N2), mouse adapted strains A/WSN/33 (H1N1), and A/PR8/34 (H1N1). We further investigated the mode of CAE action. Time-course-analysis indicated that CAE exerted its inhibition mainly at the middle stages of the replication cycle of influenza virus. Subsequently, we confirmed that CAE inhibited influenza virus RNA polymerase activity and blocked virus RNA replication and transcription in MDCK cells. In addition, we found that CAE also impaired influenza virus infectivity by directly targeting virus particles. Our data suggest that CAE is a major effective component of Cryptoporus volvatus.

ACS Style

Li Gao; Jiayuan Han; Jianyong Si; Junchi Wang; Hexiang Wang; Yipeng Sun; Yuhai Bi; Jinhua Liu; Li Cao. Cryptoporic acid E from Cryptoporus volvatus inhibits influenza virus replication in vitro. Antiviral Research 2017, 143, 106 -112.

AMA Style

Li Gao, Jiayuan Han, Jianyong Si, Junchi Wang, Hexiang Wang, Yipeng Sun, Yuhai Bi, Jinhua Liu, Li Cao. Cryptoporic acid E from Cryptoporus volvatus inhibits influenza virus replication in vitro. Antiviral Research. 2017; 143 ():106-112.

Chicago/Turabian Style

Li Gao; Jiayuan Han; Jianyong Si; Junchi Wang; Hexiang Wang; Yipeng Sun; Yuhai Bi; Jinhua Liu; Li Cao. 2017. "Cryptoporic acid E from Cryptoporus volvatus inhibits influenza virus replication in vitro." Antiviral Research 143, no. : 106-112.

Journal article
Published: 15 April 2017 in Journal of Virology
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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 countrywide outbreaks in chickens in China during 2010 to 2013, which led to the zoonotic emergence of H7N9 viruses. One of the key features of the G57 genotype is the replacement of the earlier A/chicken/Beijing/1/1994 (BJ/94)-like M gene with the A/quail/Hong Kong/G1/1997 (G1)-like M gene of quail origin. We report here 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 the BJ/94-like M gene, showed an early surge in viral mRNA and viral RNA (vRNA) transcription that was associated with enhanced viral protein production and with an early elevated release of progeny virus comprising largely spherical rather than filamentous virions. Importantly, H9N2 virus with the G1-like M gene conferred extrapulmonary virus spread in chickens. Five highly represented signature amino acid residues (37A, 95K, 224N, and 242N in the M1 protein and 21G in the M2 protein) encoded by the prevalent G1-like M gene were demonstrated to be prime contributors to enhanced infectivity. Therefore, the genetic evolution of the M gene in H9N2 virus increases reproductive virus fitness, indicating its contribution to the rising virus prevalence in chickens in China. IMPORTANCE We recently described the circulation of a dominant genotype (genotype G57) of H9N2 viruses in countrywide 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 genotype G57 H9N2 virus is the presence of the quail-origin G1-like M gene, which had replaced the earlier BJ/94-like M gene. We found that H9N2 virus with the G1-like M gene, but not the BJ/94-like M gene, showed an early surge in progeny virus production and more severe pathology and extrapulmonary virus spread in chickens. Five highly represented amino acid residues in the M1 and M2 proteins derived from the 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 in virus fitness and have implications for assessing the potential of variant influenza viruses that can cause a rising prevalence in chickens.

ACS Style

Juan Pu; Honglei Sun; Yi Qu; Chenxi Wang; Weihua Gao; Junda Zhu; Yipeng Sun; Yuhai Bi; Yinhua Huang; Kin-Chow Chang; Jie Cui; Jinhua Liu. M Gene Reassortment in H9N2 Influenza Virus Promotes Early Infection and Replication: Contribution to Rising Virus Prevalence in Chickens in China. Journal of Virology 2017, 91, e02055-16 .

AMA Style

Juan Pu, Honglei Sun, Yi Qu, Chenxi Wang, Weihua Gao, Junda Zhu, Yipeng Sun, Yuhai Bi, Yinhua Huang, Kin-Chow Chang, Jie Cui, Jinhua Liu. M Gene Reassortment in H9N2 Influenza Virus Promotes Early Infection and Replication: Contribution to Rising Virus Prevalence in Chickens in China. Journal of Virology. 2017; 91 (8):e02055-16.

Chicago/Turabian Style

Juan Pu; Honglei Sun; Yi Qu; Chenxi Wang; Weihua Gao; Junda Zhu; Yipeng Sun; Yuhai Bi; Yinhua Huang; Kin-Chow Chang; Jie Cui; Jinhua Liu. 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, no. 8: e02055-16.

Journal article
Published: 06 September 2016 in Journal of Integrative Agriculture
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H9 subtype avian influenza virus (AIV) and infectious bronchitis virus (IBV) are major pathogens circulating in poultry and have resulted in great economic losses due to respiratory disease and reduced egg production. As similar symptoms are elicited by the two pathogens, it is difficult for their differential diagnosis. So far, no reverse transcription-polymerase chain reaction (RT-PCR) assay has been found to differentiate between H9 AIV and IBV in one reaction. Therefore, developing a sensitive and specific method is of importance to simultaneously detect and differentiate H9 AIV and IBV. In this study, a duplex RT-PCR (dRT-PCR) was established. Two primer sets target the hemagglutinin (HA) gene of H9 AIV and the nucleocapsid (N) gene of IBV, respectively. Specific PCR products were obtained from all tested H9 AIVs and IBVs belonging to the major clades circulating in China, but not from AIVs of other subtypes or other infectious avian viruses. The sensitivity of the dRT-PCR assay corresponding to H9 AIV, IBV and mixture of H9 AIV and IBV were at a concentration of 1×101, 1.5×101 and 1.5×101 50% egg infective doses (EID50) mL−1, respectively. The concordance rates between the dRT-PCR and virus isolation were 99.1 and 98.2%, respectively, for detection of samples from H9N2 AIV or IBV infected chickens, while the concordance rate was 99.1% for detection of samples from H9N2 AIV and IBV co-infected chickens. Thus, the dRT-PCR assay reported herein is specific and sensitive, and suitable for the differential diagnosis of clinical infections and surveillance of H9 AIVs and IBVs.

ACS Style

Yan-Di Wei; Wei-Hua Gao; Hong-Lei Sun; Chen-Fang Yu; Xing-Yao Pei; Yi-Peng Sun; Jin-Hua Liu; Juan Pu. A duplex RT-PCR assay for detection of H9 subtype avian influenza viruses and infectious bronchitis viruses. Journal of Integrative Agriculture 2016, 15, 2105 -2113.

AMA Style

Yan-Di Wei, Wei-Hua Gao, Hong-Lei Sun, Chen-Fang Yu, Xing-Yao Pei, Yi-Peng Sun, Jin-Hua Liu, Juan Pu. A duplex RT-PCR assay for detection of H9 subtype avian influenza viruses and infectious bronchitis viruses. Journal of Integrative Agriculture. 2016; 15 (9):2105-2113.

Chicago/Turabian Style

Yan-Di Wei; Wei-Hua Gao; Hong-Lei Sun; Chen-Fang Yu; Xing-Yao Pei; Yi-Peng Sun; Jin-Hua Liu; Juan Pu. 2016. "A duplex RT-PCR assay for detection of H9 subtype avian influenza viruses and infectious bronchitis viruses." Journal of Integrative Agriculture 15, no. 9: 2105-2113.

Comparative study
Published: 15 July 2016 in Journal of Virology
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Since May 2014, highly pathogenic avian influenza H5N6 virus has been reported to cause six severe human infections three of which were fatal. The biological properties of this subtype, in particular its relative pathogenicity and transmissibility in mammals, are not known. We characterized the virus receptor-binding affinity, pathogenicity, and transmissibility in mice and ferrets of four H5N6 isolates derived from waterfowl in China from 2013-2014. All four H5N6 viruses have acquired a binding affinity for human-like SAα2,6Gal-linked receptor to be able to attach to human tracheal epithelial and alveolar cells. The emergent H5N6 viruses, which share high sequence similarity with the human isolate A/Guangzhou/39715/2014 (H5N6), were fully infective and highly transmissible by direct contact in ferrets but showed less-severe pathogenicity than the parental H5N1 virus. The present results highlight the threat of emergent H5N6 viruses to poultry and human health and the need to closely track their continual adaptation in humans. IMPORTANCE Extended epizootics and panzootics of H5N1 viruses have led to the emergence of the novel 2.3.4.4 clade of H5 virus subtypes, including H5N2, H5N6, and H5N8 reassortants. Avian H5N6 viruses from this clade have caused three fatalities out of six severe human infections in China since the first case in 2014. However, the biological properties of this subtype, especially the pathogenicity and transmission in mammals, are not known. Here, we found that natural avian H5N6 viruses have acquired a high affinity for human-type virus receptor. Compared to the parental clade 2.3.4 H5N1 virus, emergent H5N6 isolates showed less severe pathogenicity in mice and ferrets but acquired efficient in-contact transmission in ferrets. These findings suggest that the threat of avian H5N6 viruses to humans should not be ignored.

ACS Style

Honglei Sun; Juan Pu; YanDi Wei; Yipeng Sun; Jiao Hu; Litao Liu; GuanLong Xu; Weihua Gao; Chong Li; Xuxiao Zhang; Yinhua Huang; Kin-Chow Chang; Xiufan Liu; Jinhua Liu. Highly Pathogenic Avian Influenza H5N6 Viruses Exhibit Enhanced Affinity for Human Type Sialic Acid Receptor and In-Contact Transmission in Model Ferrets. Journal of Virology 2016, 90, 6235 -6243.

AMA Style

Honglei Sun, Juan Pu, YanDi Wei, Yipeng Sun, Jiao Hu, Litao Liu, GuanLong Xu, Weihua Gao, Chong Li, Xuxiao Zhang, Yinhua Huang, Kin-Chow Chang, Xiufan Liu, Jinhua Liu. Highly Pathogenic Avian Influenza H5N6 Viruses Exhibit Enhanced Affinity for Human Type Sialic Acid Receptor and In-Contact Transmission in Model Ferrets. Journal of Virology. 2016; 90 (14):6235-6243.

Chicago/Turabian Style

Honglei Sun; Juan Pu; YanDi Wei; Yipeng Sun; Jiao Hu; Litao Liu; GuanLong Xu; Weihua Gao; Chong Li; Xuxiao Zhang; Yinhua Huang; Kin-Chow Chang; Xiufan Liu; Jinhua Liu. 2016. "Highly Pathogenic Avian Influenza H5N6 Viruses Exhibit Enhanced Affinity for Human Type Sialic Acid Receptor and In-Contact Transmission in Model Ferrets." Journal of Virology 90, no. 14: 6235-6243.