Molecular determinants of virulence and stability of a reporter- expressing H5N1 influenza A virus

Journal of Virology

Volumn 89, Issue 22, 2015, Pages 11337-11346

  Zhao, Dongming ^a,b   Fukuyama, Satoshi ^a,b   Yamada, Shinya ^b   S Lopes, Tiago J ^a   Maemura, Tadashi ^b   Katsura, Hiroaki ^b   Ozawa, Makoto ^c   Watanabe, Shinji ^a,d   Neumann, Gabriele ^e   Kawaoka, Yoshihiro ^a,b,e  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KAGOSHIMA UNIVERSITY   (Japan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NA PROTEIN; NONSTRUCTURAL PROTEIN 1; PA PROTEIN; PB1 PROTEIN; PB2 PROTEIN; PROTEIN M2; UNCLASSIFIED DRUG; VIRUS PROTEIN; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A VIRUS (H5N1); M GENE; MOUSE; NA GENE; NONHUMAN; NS GENE; PA GENE; PB1 GENE; PB2 GENE; PRIORITY JOURNAL; REVERSE GENETICS; SEQUENCE ANALYSIS; VIRUS EXPRESSION; VIRUS GENE; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; C57BL MOUSE; DOG; GENETIC REASSORTMENT; GENETICS; HEK293 CELL LINE; MDCK CELL LINE; NUCLEOTIDE SEQUENCE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; REPORTER GENE; VIROLOGY; VIRULENCE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; DOGS; FEMALE; GENES, REPORTER; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; REASSORTANT VIRUSES; RNA REPLICASE; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 84945970345     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01886-15     Document Type: Article

References (49)

1. Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, Bu Z, Chen H. 2006. The NS1 gene contributes to the virulence of H5N1 avian influenza viruses. J Virol 80:11115-11123. http://dx.doi.org/10.1128/JVI.00993-06.
2. Li Y, Shi J, Zhong G, Deng G, Tian G, Ge J, Zeng X, Song J, Zhao D, Liu L, Jiang Y, Guan Y, Bu Z, Chen H. 2010. Continued evolution of H5N1 influenza viruses in wild birds, domestic poultry, and humans in China from 2004 to 2009. J Virol 84:8389-8397. http://dx.doi.org/10.1128/JVI.00413-10.
3. Neumann G, Chen H, Gao GF, Shu Y, Kawaoka Y. 2010. H5N1 influenza viruses: outbreaks and biological properties. Cell Res 20:51-61. http://dx.doi.org/10.1038/cr.2009.124.
4. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Zhang Y, Li H, Gong T, Shi Y, Ni X, Li J, Zhou J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y. 2014. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383:714-721. http://dx.doi.org/10.1016/S0140-6736(14)60111-2.
5. 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, He J, Li Q, Wang X, Gao L, Pang X, Liu G, Yan Y, Yuan H, Shu Y, Yang W, Wang Y, Wu F, Uyeki TM, Feng Z. 2014. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N Engl J Med 370:520-532. http://dx.doi.org/10.1056/NEJMoa1304617.
6. Helft J, Manicassamy B, Guermonprez P, Hashimoto D, Silvin A, Agudo J, Brown BD, Schmolke M, Miller JC, Leboeuf M, Murphy KM, Garcia-Sastre A, Merad M. 2012. Cross-presenting CD103+ dendritic cells are protected from influenza virus infection. J Clin Invest 122:4037-4047. http://dx.doi.org/10.1172/JCI60659.
7. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, Garcia-Sastre A. 2010. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc Natl Acad Sci U S A 107: 11531-11536. http://dx.doi.org/10.1073/pnas.0914994107.
8. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90. http://dx.doi.org/10.1038/nbt0102-87.
9. Fukuyama S, Katsura H, Zhao D, Ozawa M, Ando T, Shoemaker JE, Ishikawa I, Yamada S, Neumann G, Watanabe S, Kitano H, Kawaoka Y. 2015. Multi-spectral fluorescent reporter influenza viruses (Color-flu) as powerful tools for in vivo studies. Nat Commun 6:6600. http://dx.doi.org/10.1038/ncomms7600.
10. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96:9345-9350. http://dx.doi.org/10.1073/pnas.96.16.9345.
11. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918. http://dx.doi.org/10.1038/nature07745.
12. Yamayoshi S, Yamada S, Fukuyama S, Murakami S, Zhao D, Uraki R, Watanabe T, Tomita Y, Macken C, Neumann G, Kawaoka Y. 2014. Virulence-affecting amino acid changes in the PA protein of H7N9 influenza A viruses. J Virol 88:3127-3134. http://dx.doi.org/10.1128/JVI.03155-13.
13. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493-497.
14. Ozawa M, Fujii K, Muramoto Y, Yamada S, Yamayoshi S, Takada A, Goto H, Horimoto T, Kawaoka Y. 2007. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J Virol 81:30-41. http://dx.doi.org/10.1128/JVI.01434-06.
15. Murakami S, Horimoto T, Yamada S, Kakugawa S, Goto H, Kawaoka Y. 2008. Establishment of canine RNA polymerase I-driven reverse genetics for influenza A virus: its application for H5N1 vaccine production. J Virol 82:1605-1609. http://dx.doi.org/10.1128/JVI.01876-07.
16. Zhao D, Liang L, Li Y, Liu L, Guan Y, Jiang Y, Chen H. 2012. Proteomic analysis of the lungs of mice infected with different pathotypes of H5N1 avian influenza viruses. Proteomics 12:1970-1982. http://dx.doi.org/10.1002/pmic.201100619.
17. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
19. Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R, Varga ZT, Hale BG, Steel J, Perez DR, Garcia-Sastre A. 2011. Differential contribution of PB1-F2 to the virulence of highly pathogenic H5N1 influenza A virus in mammalian and avian species. PLoS Pathog 7:e1002186. http://dx.doi.org/10.1371/journal.ppat.1002186.
20. Gabriel G, Dauber B, WolffT, Planz O, Klenk HD, Stech J. 2005. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102:18590-18595. http://dx.doi.org/10.1073/pnas.0507415102.
21. Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse-Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, Webster RG, Hoffmann E. 2006. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203:689-697. http://dx.doi.org/10.1084/jem.20051938.
22. Li C, Hatta M, Watanabe S, Neumann G, Kawaoka Y. 2008. Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J Virol 82:11880-11888. http://dx.doi.org/10.1128/JVI.01445-08.
23. Leung BW, Chen H, Brownlee GG. 2010. Correlation between polymerase activity and pathogenicity in two duck H5N1 influenza viruses suggests that the polymerase contributes to pathogenicity. Virology 401:96-106. http://dx.doi.org/10.1016/j.virol.2010.01.036.
24. 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.
25. 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.
26. Suguitan AL, Jr, Matsuoka Y, Lau YF, Santos CP, Vogel L, Cheng LI, Orandle M, Subbarao K. 2012. The multibasic cleavage site of the hemagglutinin of highly pathogenic A/Vietnam/1203/2004 (H5N1) avian influenza virus acts as a virulence factor in a host-specific manner in mammals. J Virol 86:2706-2714. http://dx.doi.org/10.1128/JVI.05546-11.
27. Fan S, Deng G, Song J, Tian G, Suo Y, Jiang Y, Guan Y, Bu Z, Kawaoka Y, Chen H. 2009. Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 384:28-32. http://dx.doi.org/10.1016/j.virol.2008.11.044.
28. 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.
29. Song J, Feng H, Xu J, Zhao D, Shi J, Li Y, Deng G, Jiang Y, Li X, Zhu P, Guan Y, Bu Z, Kawaoka Y, Chen H. 2011. The PA protein directly contributes to the virulence of H5N1 avian influenza viruses in domestic ducks. J Virol 85:2180-2188. http://dx.doi.org/10.1128/JVI.01975-10.
30. Hu J, Hu Z, Song Q, Gu M, Liu X, Wang X, Hu S, Chen C, Liu H, Liu W, Chen S, Peng D, Liu X. 2013. The PA-gene-mediated lethal dissemination and excessive innate immune response contribute to the high virulence of H5N1 avian influenza virus in mice. J Virol 87:2660-2672. http://dx.doi.org/10.1128/JVI.02891-12.
31. Naffakh N, Tomoiu A, Rameix-Welti MA, van der Werf S. 2008. Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annu Rev Microbiol 62:403-424. http://dx.doi.org/10.1146/annurev.micro.62.081307.162746.
32. Obayashi E, Yoshida H, Kawai F, Shibayama N, Kawaguchi A, Nagata K, Tame JR, Park SY. 2008. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 454:1127-1131. http://dx.doi.org/10.1038/nature07225.
33. Sugiyama K, Obayashi E, Kawaguchi A, Suzuki Y, Tame JR, Nagata K, Park SY. 2009. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J 28:1803-1811. http://dx.doi.org/10.1038/emboj.2009.138.
34. He X, Zhou J, Bartlam M, Zhang R, Ma J, Lou Z, Li X, Li J, Joachimiak A, Zeng Z, Ge R, Rao Z, Liu Y. 2008. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454: 1123-1126. http://dx.doi.org/10.1038/nature07120.
35. Regan JF, Liang Y, Parslow TG. 2006. Defective assembly of influenza A virus due to a mutation in the polymerase subunit PA. J Virol 80:252-261. http://dx.doi.org/10.1128/JVI.80.1.252-261.2006.
36. Zhang H, Li X, Guo J, Li L, Chang C, Li Y, Bian C, Xu K, Chen H, Sun B. 2014. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. J Gen Virol 95:779-786. http://dx.doi.org/10.1099/vir.0.061721-0.
37. Octaviani CP, Ozawa M, Yamada S, Goto H, Kawaoka Y. 2010. High level of genetic compatibility between swine-origin H1N1 and highly pathogenic avian H5N1 influenza viruses. J Virol 84:10918-10922. http://dx.doi.org/10.1128/JVI.01140-10.
38. Zhang Y, Zhang Q, Kong H, Jiang Y, Gao Y, Deng G, Shi J, Tian G, Liu L, Liu J, Guan Y, Bu Z, Chen H. 2013. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 340:1459-1463. http://dx.doi.org/10.1126/science.1229455.
39. Sun Y, Qin K, Wang J, Pu J, Tang Q, Hu Y, Bi Y, Zhao X, Yang H, Shu Y, Liu J. 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 A 108:4164-4169. http://dx.doi.org/10.1073/pnas.1019109108.
40. Robb NC, Smith M, Vreede FT, Fodor E. 2009. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J Gen Virol 90:1398-1407. http://dx.doi.org/10.1099/vir.0.009639-0.
41. Fournier G, Chiang C, Munier S, Tomoiu A, Demeret C, Vidalain PO, Jacob Y, Naffakh N. 2014. Recruitment of RED-SMU1 complex by influenza A virus RNA polymerase to control viral mRNA splicing. PLoS Pathog 10:e1004164. http://dx.doi.org/10.1371/journal.ppat.1004164.
42. Chua MA, Schmid S, Perez JT, Langlois RA, Tenoever BR. 2013. Influenza A virus utilizes suboptimal splicing to coordinate the timing of infection. Cell Rep 3:23-29. http://dx.doi.org/10.1016/j.celrep.2012.12.010.
43. Heaton NS, Leyva-Grado VH, Tan GS, Eggink D, Hai R, Palese P. 2013. In vivo bioluminescent imaging of influenza A virus infection and characterization of novel cross-protective monoclonal antibodies. J Virol 87: 8272-8281. http://dx.doi.org/10.1128/JVI.00969-13.
44. Pan W, Dong Z, Li F, Meng W, Feng L, Niu X, Li C, Luo Q, Li Z, Sun C, Chen L. 2013. Visualizing influenza virus infection in living mice. Nat Commun 4:2369. http://dx.doi.org/10.1038/ncomms3369.
45. Kittel C, Sereinig S, Ferko B, Stasakova J, Romanova J, Wolkerstorfer A, Katinger H, Egorov A. 2004. Rescue of influenza virus expressing GFP from the NS1 reading frame. Virology 324:67-73. http://dx.doi.org/10.1016/j.virol.2004.03.035.
46. Shinya K, Fujii Y, Ito H, Ito T, Kawaoka Y. 2004. Characterization of a neuraminidase-deficient influenza A virus as a potential gene delivery vector and a live vaccine. J Virol 78:3083-3088. http://dx.doi.org/10.1128/JVI.78.6.3083-3088.2004.
47. Kreisel D, Nava RG, Li W, Zinselmeyer BH, Wang B, Lai J, Pless R, Gelman AE, Krupnick AS, Miller MJ. 2010. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc Natl Acad Sci U S A 107:18073-18078. http://dx.doi.org/10.1073/pnas.1008737107.
48. Looney MR, Thornton EE, Sen D, Lamm WJ, Glenny RW, Krummel MF. 2011. Stabilized imaging of immune surveillance in the mouse lung. Nat Methods 8:91-96. http://dx.doi.org/10.1038/nmeth.1543.
49. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.