Amino acid substitutions in polymerase basic protein 2 gene contribute to the pathogenicity of the novel A/H7N9 influenza virus in mammalian hosts

Journal of Virology

Volumn 88, Issue 6, 2014, Pages 3568-3576

  Mok, Chris Ka Pun ^a,b   Lee, Horace Hok Yeung ^a,b   Lestra, Maxime ^b   Nicholls, John Malcolm ^a   Chan, Michael Chi Wai ^a   Sia, Sin Fun ^a   Zhu, Huachen ^a   Poon, Leo Lit Man ^a   Guan, Yi ^a   Peiris, Joseph Sriyal Malik ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b HKU PASTEUR RESEARCH CENTRE   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE SEVERITY; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; FEMALE; GENE FUNCTION; GENE MUTATION; H7N9 INFLUENZA A; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA A; INFLUENZA VIRUS A H7N9; MICROBIAL KINETICS; MOUSE; NONHUMAN; PATHOGENICITY; POLYMERASE BASIC PROTEIN 2 GENE; PRIORITY JOURNAL; VIRUS REPLICATION; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; CHICKENS; CYTOKINES; FEMALE; HUMANS; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MICE; MICE, INBRED BALB C; MUTATION, MISSENSE; POULTRY DISEASES; RNA REPLICASE; VIRAL PROTEINS; VIRULENCE;

EID: 84894546931     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02740-13     Document Type: Article

References (32)

1. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. 2013. Human infection with a novel avian-origin influenza A(H7N9) virus. N. Engl. J. Med. 368:1888-1897. http://dx.doi.org/10.1056/NEJMoa1304459.
2. Yu L, Wang Z, Chen Y, Ding W, Jia H, Chan JF, To KK, Chen H, Yang Y, Liang W, Zheng S, Yao H, Yang S, Cao H, Dai X, Zhao H, Li J, Bao Q, Chen P, Hou X, Li L, Yuen KY. 2013. Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A(H7N9) virus. Clin. Infect. Dis. 57:1449-1457. http://dx.doi.org/1 0.1093/cid/cit541.
3. Ip DK, Liao Q, Wu P, Gao Z, Cao B, Feng L, Xu X, Jiang H, Li M, Bao J, Zheng J, Zhang Q, Chang Z, Li Y, Yu J, Liu F, Ni MY, Wu JT, Cowling BJ, Yang W, Leung GM, Yu H. 2013. Detection of mild to moderate influenza A/H7N9 infection by China's national sentinel surveillance system for influenza-like illness: case series. BMJ 24:f3693. http://dx.doi.org/10.1136/bmj.f3693.
4. Zhou J, Wang D, Gao R, Zhao B, Song J, Qi X, Zhang Y, Shi Y, Yang L, Zhu W, Bai T, Qin K, Lan Y, Zou S, Guo J, Dong J, Dong L, Zhang Y, Wei H, Li X, Lu J, Liu L, Zhao X, Li X, Huang W, Wen L, Bo H, Xin L, Chen Y, Xu C, Pei Y, Yang Y, Zhang X, Wang S, Feng Z, Han J, Yang W, Gao GF, Wu G, Li D, Wang Y, Shu Y. 2013. Biological features of novel avian influenza A (H7N9) virus. Nature 499:500-503. http://dx.doi.org/10.1038/nature12379.
5. Shi Y, Zhang W, Wang F, Qi J, Wu Y, Song H, Gao F, Bi Y, Zhang Y, Fan Z, Qin C, Sun H, Liu J, Haywood J, Liu W, Gong W, Wang D, Shu Y, Wang Y, Yan J, Gao GF. 2013. Structures and receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses. Science 342:243-247. http://dx.doi.org/10.1126/science.1242917.
6. Chan MCW, Chan RWY, Chan LLY, Mok CKP, Hui KPY, Fong JHM, Tao KP, Poon LLM, Nicholls JM, Guan Y, Peiris JSM. 2013. Tropism and innate host responses of a novel avian influenza A H7N9 virus: an analysis of ex-vivo and in-vitro cultures of the human respiratory tract. Lancet Respir. Med. 1:534-542. http://dx.doi.org/10.1016/S2213-2600 (13)70138-3.
7. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF. 2013. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926-1932. http://dx.doi.org/10.1016/S0140-6736(13)60938-1.
8. Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241-244. http://dx.doi.org/10.1038/nature12515.
9. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Zhang Y, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY. 2013. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381:1916-1925. http://dx.doi.org/10.1016/S0140-6736(13)60903-4.
10. Li Q, Zhou L, Zhou M, Chen Z, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, Meng L, Hong Z, Tu W, Cao Y, Li L, Ding F, Liu B, Wang M, Xie R, Gao R, Li X, Bai T, Zou S, He J, Hu J, Xu Y, Chai C, Wang S, Gao Y, Jin L, Zhang Y, Luo H, Yu H, Gao L, Pang X, Liu G, Shu Y, Yang W, Uyeki TM, Wang Y, Wu F, Feng Z. 24 April 2013. Preliminary report: epidemiology of the avian influenzaA(H7N9) outbreak in China. N. Engl. J. Med. http://dx.doi.org/10.1056/NEJMoa1304617.
11. Yang S, Chen Y, Cui D, Yao H, Lou J, Huo Z, Xie G, Yu F, Zheng S, Yang Y, Zhu Y, Lu X, Liu X, Lau SY, Chan JF, To KK, Yuen KY, Chen H, Li L. 2014. Avian-origin H7N9 virus infection in H7N9-affected areas of China: a serological study. J. Infect. Dis. 209:265-269. http://dx.doi.org/10.1093/infdis/jit430.
12. Munster VJ, de Wit E, van Riel D, Beyer WE, Rimmelzwaan GF, Osterhaus AD, Kuiken T, Fouchier RA. 2007. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J. Infect. Dis. 196:258-265. http://dx.doi.org/10.1086/518792.
13. Le QM, Sakai-Tagawa Y, Ozawa M, Ito M, Kawaoka Y. 2009. Selection of H5N1 influenza virus PB2 during replication in humans. J. Virol. 83: 5278-5281. http://dx.doi.org/10.1128/JVI.00063-09.
14. Hatta M, Gao P, Halfmann P, Kawaoka Y. 2001. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840-1842. http://dx.doi.org/10.1126/science.1062882.
15. Shinya K, Hamm S, Hatta M, Ito H, Ito T, Kawaoka Y. 2004. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320:258-266. http://dx.doi.org/10.1016/j.virol.2003.11.030.
16. Hatta M, Hatta Y, Kim JH, Watanabe S, Shinya K, Nguyen T, Lien PS, Le QM, Kawaoka Y. 2007. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog. 3:1374-1379. http://dx.doi.org/10.1371/journal.ppat.0030133.
17. Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T. 2010. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J. Virol. 84:4395-4406. http://dx.doi.org/10.1128/JVI.02642-09.
18. Yamada S, Hatta M, Staker BL, Watanabe S, Imai M, Shinya K, Sakai-Tagawa Y, Ito M, Ozawa M, Watanabe T, Sakabe S, Li C, Kim JH, Myler PJ, Phan I, Raymond A, Smith E, Stacy R, Nidom CA, Lank SM, Wiseman RW, Bimber BN, O'Connor DH, Neumann G, Stewart LJ, Kawaoka Y. 2010. Biological and structural characterization of a hostadapting amino acid in influenza virus. PLoS Pathog. 6:e1001034. http://dx.doi.org/10.1371/journal.ppat.1001034.
19. Li Z, Chen H, Jiao P, Deng G, Tian G, Li Y, Hoffmann E, Webster RG, Matsuoka Y, Yu K. 2005. Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J. Virol. 79:12058-12064. http://dx.doi.org/10.1128/JVI.79.18.12058-12064.2005.
20. Mok CK, Lee HH, Chan MC, Sia SF, Lestra M, Nicholls JM, Zhu H, Guan Y, Peiris JM. 2013. Pathogenicity of the novel A/H7N9 influenza virus in mice. mBio 4:e00362-13. http://dx.doi.org/10.1128/mBio.00362-13.
21. Tarendeau F, Crepin T, Guilligay D, Ruigrok RW, Cusack S, Hart DJ. 2008. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog. 4:e1000136. http://dx.doi.org/10.1371/journal.ppat.1000136.
22. Nicholls JM, Wong LP, Chan RW, Poon LL, So LK, Yen HL, Fung K, van Poucke S, Peiris JS. 2012. Detection of highly pathogenic influenza and pandemic influenza virus in formalin fixed tissues by immunohistochemical methods. J. Virol. Methods 179:409-413. http://dx.doi.org/10.1016/j.jviromet.2011.11.006.
23. 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. Virol. 85:9641-9645. http://dx.doi.org/10.1128/JVI.00702-11.
24. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Neumann G, Saito T, Kawaoka Y, Tashiro M. 2013. Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 18:20453. http://www.eurosurveill ance.org/ViewArticle.aspx?ArticleId=20453.
25. Zhang Y, Zhang Q, Gao Y, He X, Kong H, Jiang Y, Guan Y, Xia X, Shu Y, Kawaoka Y, Bu Z, Chen H. 2012. Key molecular factors in hemagglutinin and PB2 contribute to efficient transmission of the 2009 H1N1 pandemic influenza virus. J. Virol. 86:9666-9674. http://dx.doi.org/10.1128/JVI.00958-12.
26. Bogs J, Kalthoff D, Veits J, Pavlova S, Schwemmle M, Mänz B, Mettenleiter TC, Stech J. 2011. Reversion of PB2-627E to-627K during replication of an H5N1 clade 2.2 virus in mammalian hosts depends on the origin of the nucleoprotein. J. Virol. 85:10691-10698. http://dx.doi.org/10.1128/JVI.00786-11.
27. Yamamoto N, Sakoda Y, Okamatsu M, Kida H. 2013. Polymerase complex with lysine at position 627 of the PB2 of influenza virus A/Hong Kong/483/97 (H5N1) efficiently transcribes and replicates virus genes in mouse cells. Virus Res. 178:404-410. http://dx.doi.org/10.1016/j.virusres.2013.09.012.
28. Mehle A, Doudna JA. 2008. An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe 4:111-122. http://dx.doi.org/10.1016/j.chom.2008.06.007.
29. Moncorgé O, Mura M, Barclay WS. 2010. Evidence for avian and human host cell factors that affect the activity of influenza virus polymerase. J. Virol. 84:9978-9986. http://dx.doi.org/10.1128/JVI.01134-10.
30. Hudjetz B, Gabriel G. 2012. Human-like PB2 627K influenza virus polymerase activity is regulated by importin-α1 and-α7. PLoS Pathog. 8:e1002488. http://dx.doi.org/10.1371/journal.ppat.1002488.
31. Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E. 2005. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 79:2191-2198. http://dx.doi.org/10.1128/JVI.79.4.2191-2198.2005.
32. Chan PK, Lee N, Zaman M, Adisasmito W, Coker R, Hanshaoworakul W, Gasimov V, Oner AF, Dogan N, Tsang O, Phommasack B, Touch S, Bamgboye E, Swenson A, Toovey S, Dreyer NA. 2012. Determinants of antiviral effectiveness in influenza virus A subtype H5N1. J. Infect. Dis. 206:1359-1366. http://dx.doi.org/10.1093/infdis/jis509.