Changes in the length of the neuraminidase stalk region impact H7N9 virulence in mice

Journal of Virology

Volumn 90, Issue 4, 2016, Pages 2142-2149

  Bi, Yuhai ^a,b,e   Xiao, Haixia ^c,e   Chen, Quanjiao ^d,e   Wu, Yan ^a   Fu, Lifeng ^a   Quan, Chuansong ^f   Wong, Gary ^a   Liu, Jun ^e,f   Haywood, Joel ^a   Liu, Yingxia ^b   Zhou, Boping ^b   Yan, Jinghua ^a   Liu, Wenjun ^a,e   Gao, George ^a,b,c,e,f,g  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b SHENZHEN THIRD PEOPLE S HOSPITAL   (China)

^c Chinese Academy of Sciences   (China)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

^e INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^f CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^g ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; VIRUS SIALIDASE; CYTOKINE; NA PROTEIN, INFLUENZA A VIRUS; SIALIDASE; VIRAL PROTEIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; HUMAN; INFLUENZA A VIRUS (H7N9); NONHUMAN; PRIORITY JOURNAL; VIROGENESIS; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TITRATION; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; CYTOCHEMISTRY; GENE DELETION; GENETICS; LUNG; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; VIROLOGY; VIRULENCE; VIRUS LOAD;

ANIMALS; BODY WEIGHT; CYTOKINES; HISTOCYTOCHEMISTRY; INFLUENZA A VIRUS, H7N9 SUBTYPE; LUNG; MICE, INBRED BALB C; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; SEQUENCE DELETION; VIRAL LOAD; VIRAL PROTEINS; VIRULENCE; VIRULENCE FACTORS;

EID: 84958063906     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02553-15     Document Type: Article

References (27)

1. Muramoto Y, Noda T, Kawakami E, Akkina R, Kawaoka Y. 2013. Identification of novel influenza A virus proteins translated from PA mRNA. J Virol 87:2455-2462. http://dx.doi.org/10.1128/JVI.02656-12.
2. Shi Y, Wu Y, Zhang W, Qi J, Gao GF. 2014. Enabling the 'host jump': structural determinants of receptor-binding specificity in influenza A viruses. Nat Rev Microbiol 12:822-831. http://dx.doi.org/10.1038/nrmicro3362.
3. Kawaoka Y, Webster RG. 1988. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells. Proc Natl Acad Sci U S A 85:324-328. http://dx.doi.org/10.1073/pnas.85.2.324.
4. Steinhauer DA. 1999. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258:1-20. http://dx.doi.org/10.1006/viro.1999.9716.
5. Zhang Y, Sun YP, Sun HL, Pu J, Bi YH, Shi Y, Lu XS, Li J, Zhu QY, Gao GF, Yang HC, Liu JH. 2012. A single amino acid at the hemagglutinin cleavage site contributes to the pathogenicity and neurovirulence of H5N1 influenza virus in mice. J Virol 86:6924-6931. http://dx.doi.org/10.1128/JVI.07142-11.
6. 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, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, 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.
7. Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, Yamada S, Murakami S, Yamayoshi S, Iwatsuki-Horimoto K, Sakoda Y, Takashita E, McBride R, Noda T, Hatta M, Imai H, Zhao D, Kishida N, Shirakura M, De Vries RP, Shichinohe S, Okamatsu M, Tamura T, Tomita Y, Fujimoto N, Goto K, Katsura H, Kawakami E, Ishikawa I, Watanabe S, Ito M, Sakai-Tagawa Y, Sugita Y, Uraki R, Yamaji R, Eisfeld AJ, Zhong G, Fan S, Ping J, Maher EA, Hanson A, Uchida Y, Saito T, Ozawa M, Neumann G, Kida H, Odagiri T, Paulson JC, Hasegawa H, Tashiro M, Kawaoka Y. 2013. Characterization of H7N9 influenza A viruses isolated from humans. Nature 501:551-555. http://dx.doi.org/10.1038/nature12392.
8. Matrosovich M, Zhou N, Kawaoka Y, Webster R. 1999. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73:1146-1155.
9. Matsuoka Y, Swayne DE, Thomas C, Rameix-Welti MA, Naffakh N, Warnes C, Altholtz M, Donis R, Subbarao K. 2009. Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. J Virol 83:4704-4708. http://dx.doi.org/10.1128/JVI.01987-08.
10. Banks J, Speidel ES, Moore E, Plowright L, Piccirillo A, Capua I, Cordioli P, Fioretti A, Alexander DJ. 2001. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 146:963-973. http://dx.doi.org/10.1007/s007050170128.
11. Campitelli L, Mogavero E, De Marco MA, Delogu M, Puzelli S, Frezza F, Facchini M, Chiapponi C, Foni E, Cordioli P, Webby R, Barigazzi G, Webster RG, Donatelli I. 2004. Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 323:24-36. http://dx.doi.org/10.1016/j.virol.2004.02.015.
12. Sun YP, Tan YY, Wei K, Sun HL, Shi Y, Pu J, Yang HC, Gao GF, Yin YB, Feng WH, Perez DR, Liu JH. 2013. Amino acid 316 of hemagglutinin and the neuraminidase stalk length influence virulence of H9N2 influenza virus in chickens and mice. J Virol 87:2963-2968. http://dx.doi.org/10.1128/JVI.02688-12.
13. Zhou H, Yu Z, Hu Y, Tu J, Zou W, Peng Y, Zhu J, Li Y, Zhang A, Ye Z, Chen H, Jin M. 2009. The special neuraminidase stalk-motif responsible for increased virulence and pathogenesis of H5N1 influenza A virus. PLoS One 4:e6277. http://dx.doi.org/10.1371/journal.pone.0006277.
14. 2 influenza A virus in the respiratory tract of chickens. J Virol 84:11831-11840. http://dx.doi.org/10.1128/JVI.01460-10.
15. Munier S, Larcher T, Cormier-Aline F, Soubieux D, Su B, Guigand L, Labrosse B, Cherel Y, Quere P, Marc D, Naffakh N. 2010. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol 84:940-952. http://dx.doi.org/10.1128/JVI.01581-09.
16. Blumenkrantz D, Roberts KL, Shelton H, Lycett S, Barclay WS. 2013. The short stalk length of highly pathogenic avian influenza H5N1 virus neuraminidase limits transmission of pandemic H1N1 virus in ferrets. J Virol 87:10539-10551. http://dx.doi.org/10.1128/JVI.00967-13.
17. Luo G, Chung J, Palese P. 1993. Alterations of the stalk of the influenza virus neuraminidase: deletions and insertions. Virus Res 29:321. http://dx.doi.org/10.1016/0168-1702(93)90069-Y.
18. Mitnaul LJ, Matrosovich MN, Castrucci MR, Tuzikov AB, Bovin NV, Kobasa D, Kawaoka Y. 2000. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J Virol 74:6015-6020. http://dx.doi.org/10.1128/JVI.74.13.6015-6020.2000.
19. Xu R, Zhu X, McBride R, Nycholat CM, Yu W, Paulson JC, Wilson IA. 2012. Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic. J Virol 86:9221-9232. http://dx.doi.org/10.1128/JVI.00697-12.
20. Casalegno JS, Ferraris O, Escuret V, Bouscambert M, Bergeron C, Lines L, Excoffier T, Valette M, Frobert E, Pillet S, Pozzetto B, Lina B, Ottmann M. 2014. Functional balance between the hemagglutinin and neuraminidase of influenza A(H1N1)pdm09 HA D222 variants. PLoS One 9:e104009. http://dx.doi.org/10.1371/journal.pone.0104009.
21. Gen F, Yamada S, Kato K, Akashi H, Kawaoka Y, Horimoto T. 2013. Attenuation of an influenza A virus due to alteration of its hemagglutininneuraminidase functional balance in mice. Arch Virol 158:1003-1011. http://dx.doi.org/10.1007/s00705-012-1577-3.
22. Lu B, Zhou H, Ye D, Kemble G, Jin H. 2005. Improvement of influenza A/Fujian/411/02 (H3N2) virus growth in embryonated chicken eggs by balancing the hemagglutinin and neuraminidase activities, using reverse genetics. J Virol 79:6763-6771. http://dx.doi.org/10.1128/JVI.79.11.6763-6771.2005.
23. Yen HL, Liang CH, Wu CY, Forrest HL, Ferguson A, Choy KT, Jones J, Wong DD, Cheung PP, Hsu CH, Li OT, Yuen KM, Chan RW, Poon LL, Chan MC, Nicholls JM, Krauss S, Wong CH, Guan Y, Webster RG, Webby RJ, Peiris M. 2011. Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets. Proc Natl Acad Sci U S A 108:14264-14269. http://dx.doi.org/10.1073/pnas.1111000108.
24. Bi Y, Xie Q, Zhang S, Li Y, Xiao H, Jin T, Zheng W, Li J, Jia X, Sun L, Liu J, Qin C, Gao GF, Liu W. 2015. Assessment of the internal genes of influenza A (H7N9) virus contributing to the high pathogenicity in mice. J Virol 89:2-13. http://dx.doi.org/10.1128/JVI.02390-14.
25. Wu Y, Bi Y, Vavricka CJ, Sun X, Zhang Y, Gao F, Zhao M, Xiao H, Qin C, He J, Liu W, Yan J, Qi J, Gao GF. 2013. Characterization of two distinct neuraminidases from avian-origin human-infecting H7N9 influenza viruses. Cell Res 23:1347-1355. http://dx.doi.org/10.1038/cr.2013.144.
26. Zhang WJ, Xue T, Wu XW, Zhang PH, Zhao G, Peng DX, Hu SL, Wang XQ, Liu XW, Liu WB, Liu XF. 2011. Increase in viral yield in eggs and MDCK cells of reassortant H5N1 vaccine candidate viruses caused by insertion of 38 amino acids into the NA stalk. Vaccine 29:8032-8041. http://dx.doi.org/10.1016/j.vaccine.2011.08.054.
27. 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 One 3:e3170. http://dx.doi.org/10.1371/journal.pone.0003170.