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Abstract
The recent human infection with avian influenza virus revealed that H9N2 influenza virus is the gene donor for H7N9 and H10N8 viruses infecting humans. The crucial role of H9N2 viruses at the animal-human interface might be due to the wide host range, adaptation in both poultry and mammalian, and extensive gene reassortment. As the most prevalent subtype of influenza viruses in chickens in China, H9N2 also causes a great economic loss for the poultry industry, even under the long-term vaccination programs. The history, epidemiology, biological characteristics, and molecular determinants of H9N2 influenza virus are reviewed in this paper. The contribution of H9N2 genes, especially RNP genes, to the infection of humans needs to be investigated in the future.
Keywords
Influenza
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Poultry
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H9N2
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Evolution
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Virulence
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Antigenic drift
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Yipeng Sun, Jinhua Liu.
H9N2 influenza virus in China: a cause of concern.
Protein Cell, 2015, 6(1): 18-25 DOI:10.1007/s13238-014-0111-7
| [1] |
Bi J, Deng G, Dong J, Kong F, Li X, Xu Q, Zhang M, Zhao L, Qiao J (2010) Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007-2009. PLoS One5: e13063
|
| [2] |
Bonfante F, Patrono LV, Aiello R, Beato MS, Terregino C, Capua I (2013) Susceptibility and intra-species transmission of the H9N2 G1 prototype lineage virus in Japanese quail and turkeys. Vet Microbiol165: 177-183
|
| [3] |
Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol43: 5760-5767
|
| [4] |
Chen BL, Zhang Z, Chen WB (1994) The study of avian influenza: I. The isolation and preliminary serological identification of avian influenza virus in chicken. Chin J Vet Med20: 3-5
|
| [5] |
Chen F, Chen XC (1999) The genetic analysis of Avian influenza A/chicken/Beijing/1/96 (H9N2) strain. Chin J Vet Med21: 130-133
|
| [6] |
Cong YL, Pu J, Liu QF, Wang S, Zhang GZ, Zhang XL, Fan WX, Brown EG, Liu JH (2007) Antigenic and genetic characterization of H9N2 swine influenza viruses in China. J Gen Virol88: 2035-2041
|
| [7] |
Cui L, Liu D, Shi W, Pan J, Qi X, Li X, Guo X, Zhou M, Li W, Li J (2014) Dynamic reassortments and genetic heterogeneity of the human-infecting influenza A (H7N9) virus. Nat Commun5: 3142
|
| [8] |
Deng G, Bi J, Kong F, Li X, Xu Q, Dong J, Zhang M, Zhao L, Luan Z, Lv N (2010) Acute respiratory distress syndrome induced by H9N2 virus in mice. Archiv Virol155: 187-195
|
| [9] |
Guan Y, Shortridge KF, Krauss S, Webster RG (1999) Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA96: 9363-9367
|
| [10] |
Guo Y, Li J, Cheng X (1999) [Discovery of men infected by avian influenza A (H9N2) virus]. Zhonghua shi yan he lin chuang bing du xue za zhi= Zhonghua shiyan he linchuang bingduxue zazhi=. Chin J Exp Clin Virol13: 105-108
|
| [11] |
Guo Y, Xie J, Wang M (2000) [A strain of influenza A H9N2 virus repeatedly isolated from human population in China]. Zhonghua shi yan he lin chuang bing du xue za zhi= Zhonghua shiyan he linchuang bingduxue zazhi=. Chin J Exp Clin Virol14: 209-212
|
| [12] |
Guo Y, Xie J, Wu K, Dong J, Wang M, Zhang Y, Guo J, Chen J, Chen Z, Li Z (2002) [Characterization of genome of A/Guangzhou/333/ 99(H9N2) virus]. Zhonghua shi yan he lin chuang bing du xue za zhi= Zhonghua shiyan he linchuang bingduxue zazhi=. Chin J Exp Clin Virol16: 142-145
|
| [13] |
Ha Y, Stevens DJ, Skehel JJ, Wiley DC (2001) X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci USA98: 11181-11186
|
| [14] |
Hossain MJ, Hickman D, Perez DR (2008) Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One3: e3170
|
| [15] |
Huang R, Wang AR, Liu ZH, Liang W, Li XX, Tang YJ, Miao ZM, Chai TJ (2013) Seroprevalence of avian influenza H9N2 among poultry workers in Shandong Province, China. Eur J Clin Microbiol Infect Dis32: 1347-1351
|
| [16] |
Kaverin NV, Rudneva IA, Ilyushina NA, Lipatov AS, Krauss S, Webster RG (2004) Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. J Virol78: 240-249
|
| [17] |
Kimble JB, Sorrell E, Shao H, Martin PL, Perez DR (2011) Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci U S A108: 12084-12088
|
| [18] |
Kimble JB, Angel M, Wan H, Sutton TC, Finch C, Perez DR (2014) Alternative reassortment events leading to transmissible H9N1 influenza viruses in the ferret model. J Virol88: 66-71
|
| [19] |
Ku KB, Park EH, Yum J, Kim HM, Kang YM, Kim JC, Kim JA, Kim HS, Seo SH (2014) Transmissibility of novel H7N9 and H9N2 avian influenza viruses between chickens and ferrets. Virology450-451: 316-323
|
| [20] |
Lee DH, Song CS (2013) H9N2 avian influenza virus in Korea: evolution and vaccination. Clin Exp Vaccine Res2: 26-33
|
| [21] |
Li C, Yu K, Tian G, Yu D, Liu L, Jing B, Ping J, Chen H (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology340: 70-83
|
| [22] |
Liu KY (2012) Epidemicity and control of H9N2 subtype avian influenza virus. Anim Husb Feed Sci33: 116
|
| [23] |
Liu D, Shi W, Gao GF (2014) Poultry carrying H9N2 act as incubators for novel human avian influenza viruses. Lancet383: 869
|
| [24] |
Lv J, Wei B, Yang Y, Yao M, Cai Y, Gao Y, Xia X, Zhao X, Liu Z, Li X (2012) Experimental transmission in guinea pigs of H9N2 avian influenza viruses from indoor air of chicken houses. Virus Res170: 102-108
|
| [25] |
Mok CK, Yen HL, Yu MY, Yuen KM, Sia SF, Chan MC, Qin G, Tu WW, Peiris JS (2011) Amino acid residues 253 and 591 of the PB2 protein of avian influenza virus A H9N2 contribute to mammalian pathogenesis. J Virol85: 9641-9645
|
| [26] |
Okamatsu M, Sakoda Y, Kishida N, Isoda N, Kida H (2008) Antigenic structure of the hemagglutinin of H9N2 influenza viruses. Archiv Virol153: 2189-2195
|
| [27] |
Pan Q, Liu A, Zhang F, Ling Y, Ou C, Hou N, He C (2012) Coinfection of broilers with Ornithobacterium rhinotracheale and H9N2 avian influenza virus. BMC vet Res8: 104
|
| [28] |
Peiris JS, Guan Y, Markwell D, Ghose P, Webster RG, Shortridge KF (2001) Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol75: 9679-9686
|
| [29] |
Saito T, Lim W, Suzuki T, Suzuki Y, Kida H, Nishimura SI, Tashiro M (2001) Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine20: 125-133
|
| [30] |
Shanmuganatham K, Feeroz MM, Jones-Engel L, Smith GJ, Fourment M, Walker D, McClenaghan L, Alam SM, Hasan MK, Seiler P. (2013) Antigenic and molecular characterization of avian influenza A(H9N2) viruses, Bangladesh. Emerg Infect Dis19
|
| [31] |
Shi W, Li W, Li X, Haywood J, Ma J, Gao GF, Liu D (2014) Phylogenetics of varied subtypes of avian influenza viruses in China: potential threat to humans. Protein Cell5: 253-257
|
| [32] |
Sorrell EM, Wan H, Araya Y, Song H, Perez DR (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A106: 7565-7570
|
| [33] |
Subbarao K, Katz J (2000) Avian influenza viruses infecting humans. Cell Mol Life Sci CMLS57: 1770-1784
|
| [34] |
Sun Y, Bi Y, Pu J, Hu Y, Wang J, Gao H, Liu L, Xu Q, Tan Y, Liu M (2010a) Guinea pig model for evaluating the potential public health risk of swine and avian influenza viruses. PLoS One: e15537
|
| [35] |
Sun Y, Pu J, Jiang Z, Guan T, Xia Y, Xu Q, Liu L, Ma B, Tian F, Brown EG (2010b) Genotypic evolution and antigenic drift of H9N2 influenza viruses in China from 1994 to 2008. Vet Microbiol146: 215-225
|
| [36] |
Sun Y, Qin K, Wang J, Pu J, Tang Q, Hu Y, Bi Y, Zhao X, Yang H, Shu Y (2011) High genetic compatibility and increased pathogenicity of reassortants derived from avian H9N2 and pandemic H1N1/2009 influenza viruses. Proc Natl Acad Sci U S A108: 4164-4169
|
| [37] |
Sun Y, Pu J, Fan L, Sun H, Wang J, Zhang Y, Liu L, Liu J (2012) Evaluation of the protective efficacy of a commercial vaccine against different antigenic groups of H9N2 influenza viruses in chickens. Vet Microbiol: 193-199
|
| [38] |
Sun X, Xu X, Liu Q, Liang D, Li C, He Q, Jiang J, Cui Y, Li J, Zheng L (2013a) Evidence of avian-like H9N2 influenza A virus among dogs in Guangxi, China. Infect Genet Evol: J Mol Epidemiol Evol Genet Infect Dis20: 471-475
|
| [39] |
Sun Y, Tan Y, Wei K, Sun H, Shi Y, Pu J, Yang H, Gao GF, Yin Y, Feng W (2013b) Amino acid 316 of hemagglutinin and the neuraminidase stalk length influence virulence of H9N2 influenza virus in chickens and mice. J Virol87: 2963-2968
|
| [40] |
Uyeki TM, Chong YH, Katz JM, Lim W, Ho YY, Wang SS, Tsang TH, Au WW, Chan SC, Rowe T (2002) Lack of evidence for human-to-human transmission of avian influenza A (H9N2) viruses in Hong Kong, China 1999. Emerg Infect Dis8: 154-159
|
| [41] |
Wan H, Perez DR(2007) Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol81: 5181-5191
|
| [42] |
Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I, Stevens J, Cattoli G, Capua I, Chen LM (2008) Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One3: e2923
|
| [43] |
Wan Z, Ye J, Xu L, Shao H, Jin W, Qian K, Wan H, Qin A (2014) Antigenic mapping of the hemagglutinin of an H9N2 avian influenza virus reveals novel critical amino acid positions in antigenic sites. J Virol88: 3898-3901
|
| [44] |
Wang B, Chen Q, Chen Z (2012a) Complete genome sequence of an H9N2 avian influenza virus isolated from egret in Lake Dongting wetland. J Virol86: 11939
|
| [45] |
Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J (2012b) Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One7: e40752
|
| [46] |
Wang Q, Ju L, Liu P, Zhou J, Lv X, Li L, Shen H, Su H, Jiang L, Jiang Q (2014) Serological and virological surveillance of avian influenza A virus H9N2 subtype in humans and poultry in Shanghai, China, between 2008 and 2010. Zoonoses Public Health.
|
| [47] |
Wu R, Zhang H, Yang K, Liang W, Xiong Z, Liu Z, Yang X, Shao H, Zheng X, Chen M (2009) Multiple amino acid substitutions are involved in the adaptation of H9N2 avian influenza virus to mice. Vet Microbiol138: 85-91
|
| [48] |
Wu A, Su C, Wang D, Peng Y, Liu M, Hua S, Li T, Gao GF, Tang H, Chen J (2013) Sequential reassortments underlie diverse influenza H7N9 genotypes in China. Cell Host Microbe14: 446-452
|
| [49] |
Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D, Wang J, Zhang JX, Li KS, Fan XH (2007) The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol81: 10389-10401
|
| [50] |
Yu Q, Liu L, Pu J, Zhao J, Sun Y, Shen G, Wei H, Zhu J, Zheng R, Xiong D (2013) Risk perceptions for avian influenza virus infection among poultry workers, China. Emerg Infect Dis19: 313-316
|
| [51] |
Zhang GZJ (2013) The analysis of epidemic diseases in poultry in 2013 China Poultry35: 56-59
|
| [52] |
Zhang ZJ, Chen B, Chen WB (1994) The study of avian influenza: II. The incidence and serological survey of avian influenza. Chin J Vet Med20: 6-7
|
| [53] |
Zhang P, Tang Y, Liu X, Peng D, Liu W, Liu H, Lu S, Liu X (2008) Characterization of H9N2 influenza viruses isolated from vaccinated flocks in an integrated broiler chicken operation in eastern China during a 5 year period (1998-2002). J Gen Virol89: 3102-3112
|
| [54] |
Zhang K, Xu W, Zhang Z, Wang T, Sang X, Cheng K, Yu Z, Zheng X, Wang H, Zhao Y (2013a) Experimental infection of nonhuman primates with avian influenza virus (H9N2). Archiv Virol158: 2127-2134
|
| [55] |
Zhang K, Zhang Z, Yu Z, Li L, Cheng K, Wang T, Huang G, Yang S, Zhao Y, Feng N (2013b) Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Res175: 52-57
|
| [56] |
Zhao M, Liu Q, Sun Q, Zhang W, Zhao G, Gu M, Wang X, Hu S, Liu X, Liu X (2013) Full genome sequence of a natural reassortant H9N2 Avian influenza virus isolated from domestic ducks in Jiangsu Province, China. Genome Announc1: e00463-13
|
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