Influenza A and B virus intertypic reassortment through compatible viral packaging signals

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10778-10791

  Baker, Steven F ^a   Nogales, Aitor ^a   Finch, Courtney ^c   Tuffy, Kevin M ^a   Domm, William ^a   Perez, Daniel R ^c   Topham, David J ^a,b   Martínez Sobrido, Luis ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDYLTRANSFERASE; POLYMERASE; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS HEMAGGLUTININ; VIRUS SIALIDASE; INFLUENZA VIRUS HEMAGGLUTININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME SPECIFICITY; FEMALE; GENE EXPRESSION; GENETIC COMPATIBILITY; GENETIC REASSORTMENT; HUMAN; HUMAN CELL; IMMUNOGENICITY; INFLUENZA VIRUS A; INFLUENZA VIRUS B; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SPECIES DIFFERENTIATION; TRANSGENE; VIRAL PACKAGING SIGNAL; VIRAL PHENOMENA AND FUNCTIONS; VIRION; VIRUS GENOME; VIRUS RELEASE; VIRUS REPLICATION; VIRUS VIRULENCE; CHEMISTRY; GENETIC RECOMBINATION; GENETICS; INFLUENZA; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ASSEMBLY;

HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; INFLUENZA, HUMAN; REASSORTANT VIRUSES; RECOMBINATION, GENETIC; VIRUS ASSEMBLY;

EID: 84906334033     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01440-14     Document Type: Article

References (82)

1. Palese P, Shaw ML. 2007. Orthomyxoviridae: the viruses and their replication. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Chen R, Holmes EC. 2008. The evolutionary dynamics of human influenza B virus. J. Mol. Evol. 66:655-663. http://dx.doi.org/10.1007/s00239 -008-9119-z.
3. Osterhaus AD, Rimmelzwaan GF, Martina BE, Bestebroer TM, Fouchier RA. 2000. Influenza B virus in seals. Science 288:1051-1053. http://dx.doi.org/10.1126/science.288.5468.1051.
4. Baker SF, Guo H, Albrecht RA, Garcia-Sastre A, Topham DJ, Martinez- Sobrido L. 2013. Protection against lethal influenza with a viral mimic. J. Virol. 87:8591-8605. http://dx.doi.org/10.1128/JVI.01081-13.
5. Jackson D, Elderfield RA, Barclay WS. 2011. Molecular studies of influenza B virus in the reverse genetics era. J. Gen. Virol. 92:1-17. http://dx .doi.org/10.1099/vir.0.026187-0.
6. Schild GC, Oxford JS, de Jong JC, Webster RG. 1983. Evidence for host-cell selection of influenza virus antigenic variants. Nature 303:706-709. http://dx.doi.org/10.1038/303706a0.
7. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO. 2012. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 109:4269-4274. http://dx.doi.org/10.1073/pnas.1116200109.
8. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. 2013. New World bats harbor diverse influenza A viruses. PLoS Pathog. 9:e1003657. http://dx.doi.org/10.1371/journal.ppat.1003657.
9. McCullers JA, Saito T, Iverson AR. 2004. Multiple genotypes of influenza B virus circulated between 1979 and 2003. J. Virol. 78:12817-12828. http: //dx.doi.org/10.1128/JVI.78.23.12817-12828.2004.
10. Rota P, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K. 1990. Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 175:59-68. http://dx.doi.org/10.1016/0042 -6822(90)90186-U.
11. Kanegae Y, Sugita S, Endo A, Ishida M, Senya S, Osako K, Nerome K, Oya A. 1990. Evolutionary pattern of the hemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season. J. Virol. 64:2860-2865.
12. McCullers JA, Wang GC, He S, Webster RG. 1999. Reassortment and insertion-deletion are strategies for the evolution of influenza B viruses in nature. J. Virol. 73:7343-7348.
13. Xu X, Lindstrom SE, Shaw MW, Smith CB, Hall HE, Mungall BA, Subbarao K, Cox NJ, Klimov A. 2004. Reassortment and evolution of current human influenza A and B viruses. Virus Res. 103:55-60. http://dx .doi.org/10.1016/j.virusres.2004.02.013.
14. Mikheeva A, Ghendon YZ. 1982. Intrinsic interference between influenza A and B viruses. Arch. Virol. 73:287-294. http://dx.doi.org/10.1007 /BF01318082.
15. Kaverin NV, Varich NL, Sklyanskaya EI, Amvrosieva TV, Petrik J, Vovk TC. 1983. Studies on heterotypic interference between influenza A and B viruses: a differential inhibition of the synthesis of viral proteins and RNAs. J. Gen. Virol. 64(Pt 10):2139-2146.
16. Tobita K, Tanaka T, Goto H, Feng SY. 1983. Temperature-sensitive influenza A virus clones originated by a cross between A/Aichi/2/68 (H3N2) and B/Yamagata/1/73. Arch. Virol. 75:17-27. http://dx.doi.org /10.1007/BF01314124.
17. Ghate AA, Air GM. 1999. Influenza type B neuraminidase can replace the function of type A neuraminidase. Virology 264:265-277. http://dx.doi .org/10.1006/viro.1999.9936.
18. Flandorfer A, Garcia-Sastre A, Basler CF, Palese P. 2003. Chimeric influenza A viruses with a functional influenza B virus neuraminidase or hemagglutinin. J. Virol. 77:9116-9123. http://dx.doi.org/10.1128/JVI.77 .17.9116-9123.2003.
19. Horimoto T, Takada A, Iwatsuki-Horimoto K, Hatta M, Goto H, Kawaoka Y. 2003. Generation of influenza A viruses with chimeric (type A/B) hemagglutinins. J. Virol. 77:8031-8038. http://dx.doi.org/10.1128 /JVI.77.14.8031-8038.2003.
20. Muster T, Subbarao EK, Enami M, Murphy BR, Palese P. 1991. An influenzaAvirus containing influenza B virus 5= and 3= noncoding regions on the neuraminidase gene is attenuated in mice. Proc. Natl. Acad. Sci. U. S. A. 88:5177-5181. http://dx.doi.org/10.1073/pnas.88.12.5177.
21. Crescenzo-Chaigne B, Naffakh N, van der Werf S. 1999. Comparative analysis of the ability of the polymerase complexes of influenza viruses type A, B and C to assemble into functional RNPs that allow expression and replication of heterotypic model RNA templates in vivo. Virology 265:342-353. http://dx.doi.org/10.1006/viro.1999.0059.
22. Iwatsuki-Horimoto K, Hatta Y, Hatta M, Muramoto Y, Chen H, Kawaoka Y, Horimoto T. 2008. Limited compatibility between the RNA polymerase components of influenza virus type A and B. Virus Res. 135: 161-165. http://dx.doi.org/10.1016/j.virusres.2008.03.010.
23. Fodor E, Pritlove DC, Brownlee GG. 1994. The influenza virus panhandle is involved in the initiation of transcription. J. Virol. 68:4092-4096.
24. Stoeckle MY, Shaw MW, Choppin PW. 1987. Segment-specific and common nucleotide sequences in the noncoding regions of influenza B virus genome RNAs. Proc. Natl. Acad. Sci. U. S. A. 84:2703-2707. http: //dx.doi.org/10.1073/pnas.84.9.2703.
25. Hutchinson EC, von Kirchbach JC, Gog JR, Digard P. 2010. Genome packaging in influenza A virus. J. Gen. Virol. 91:313-328. http://dx.doi .org/10.1099/vir.0.017608-0.
26. Martinez-Sobrido L, Cadagan R, Steel J, Basler CF, Palese P, Moran TM, Garcia-Sastre A. 2010. Hemagglutinin-pseudotyped green fluorescent protein-expressing influenza viruses for the detection of influenza virus neutralizing antibodies. J. Virol. 84:2157-2163. http://dx.doi.org/10 .1128/JVI.01433-09.
27. Fujii Y, Goto H, Watanabe T, Yoshida T, Kawaoka Y. 2003. Selective incorporation of influenza virusRNAsegments into virions. Proc. Natl. Acad. Sci. U. S. A. 100:2002-2007. http://dx.doi.org/10.1073/pnas.0437772100.
28. Marsh GA, Hatami R, Palese P. 2007. Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J. Virol. 81:9727-9736. http://dx.doi.org/10.1128/JVI .01144-07.
29. Rodrigo WW, de la Torre JC, Martinez-Sobrido L. 2011. Use of singlecycle infectious lymphocytic choriomeningitis virus to study hemorrhagic fever arenaviruses. J. Virol. 85:1684-1695. http://dx.doi.org/10.1128/JVI .02229-10.
30. Martinez-Sobrido L, Garcia-Sastre A. 2010. Generation of recombinant influenza virus from plasmid DNA. J. Vis. Exp. 3:2057. http://dx.doi.org /10.3791/2057.
31. Schickli JH, Flandorfer A, Nakaya T, Martinez-Sobrido L, Garcia-Sastre A, Palese P. 2001. Plasmid-only rescue of influenza A virus vaccine candidates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:1965-1973. http://dx .doi.org/10.1098/rstb.2001.0979.
32. Hai R, Martinez-Sobrido L, Fraser KA, Ayllon J, Garcia-Sastre A, Palese P. 2008. Influenza B virus NS1-truncated mutants: live-attenuated vaccine approach. J. Virol. 82:10580-10590. http://dx.doi.org/10.1128/JVI .01213-08.
33. Hai R, Schmolke M, Varga ZT, Manicassamy B, Wang TT, Belser JA, Pearce MB, Garcia-Sastre A, Tumpey TM, Palese P. 2010. PB1-F2 expression by the 2009 pandemic H1N1 influenza virus has minimal impact on virulence in animal models. J. Virol. 84:4442-4450. http://dx.doi .org/10.1128/JVI.02717-09.
34. Hoffmann E, Neumann G, Hobom G, Webster RG, Kawaoka Y. 2000. "Ambisense" approach for the generation of influenza A virus: vRNA and mRNA synthesis from one template. Virology 267:310-317. http://dx.doi .org/10.1006/viro.1999.0140.
35. Fodor E, Devenish L, Engelhardt OG, Palese P, Brownlee GG, Garcia- Sastre A. 1999. Rescue of influenza A virus from recombinant DNA. J. Virol. 73:9679-9682.
36. Kilbourne ED. 1969. Future influenza vaccines and the use of genetic recombinants. Bull. World Health Organ. 41:643-645.
37. Pena L, Sutton T, Chockalingam A, Kumar S, Angel M, Shao H, Chen H, Li W, Perez DR. 2013. Influenza viruses with rearranged genomes as live-attenuated vaccines. J. Virol. 87:5118-5127. http://dx.doi.org/10 .1128/JVI.02490-12.
38. Chapman TJ, Castrucci MR, Padrick RC, Bradley LM, Topham DJ. 2005. Antigen-specific and non-specific CD4+ T cell recruitment and proliferation during influenza infection. Virology 340:296-306. http://dx .doi.org/10.1016/j.virol.2005.06.023.
39. O'Neill RE, Talon J, Palese P. 1998. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins.EMBOJ. 17:288-296. http://dx.doi.org/10.1093/emboj/17.1.288.
40. Bauman JD, Patel D, Baker SF, Vijayan RS, Xiang A, Parhi AK, Martinez-Sobrido L, LaVoie EJ, Das K, Arnold E. 2013. Crystallographic fragment screening and structure-based optimization yields a new class of influenza endonuclease inhibitors. ACS Chem. Biol. 8:2501-2508. http: //dx.doi.org/10.1021/cb400400j.
41. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146:2275-2289. http://dx.doi.org/10.1007/s007050170002.
42. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 97:6108-6113. http://dx.doi.org /10.1073/pnas.100133697.
43. Song H, Nieto GR, Perez DR. 2007. A new generation of modified live-attenuated avian influenza viruses using a two-strategy combination as potential vaccine candidates. J. Virol. 81:9238-9248. http://dx.doi.org /10.1128/JVI.00893-07.
44. Hoffmann E, Mahmood K, Yang CF, Webster RG, Greenberg HB, Kemble G. 2002. Rescue of influenza B virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 99:11411-11416. http://dx.doi.org/10.1073/pnas .172393399.
45. Mayer D, Molawi K, Martinez-Sobrido L, Ghanem A, Thomas S, Baginsky S, Grossmann J, Garcia-Sastre A, Schwemmle M. 2007. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 6:672-682. http://dx.doi.org/10.1021/pr060432u.
46. Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC. 2006. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 80:9192-9199. http://dx.doi.org/10.1128/JVI.00555-06.
47. Rimmelzwaan GF, Nieuwkoop NJ, de Mutsert G, Boon AC, Kuiken T, Fouchier RA, Osterhaus AD. 2007. Attachment of infectious influenza A viruses of various subtypes to live mammalian and avian cells as measured by flow cytometry. Virus Res. 129:175-181. http://dx.doi.org/10.1016/j .virusres.2007.07.007.
48. Medina RA, Manicassamy B, Stertz S, Seibert CW, Hai R, Belshe RB, Frey SE, Basler CF, Palese P, Garcia-Sastre A. 2010. Pandemic 2009 H1N1 vaccine protects against 1918 Spanish influenza virus. Nat. Commun. 1:28. http://dx.doi.org/10.1038/ncomms1026.
49. Reale MA, Manheimer AJ, Moran TM, Norton G, Bona CA, Schulman JL. 1986. Characterization of monoclonal antibodies specific for sequential influenza A/PR/8/34 virus variants. J. Immunol. 137:1352-1358.
50. Ortiz-Riano E, Cheng BY, de la Torre JC, Martinez-Sobrido L. 2011. The C-terminal region of lymphocytic choriomeningitis virus nucleoprotein contains distinct and segregable functional domains involved in NP-Z interaction and counteraction of the type I interferon response. J. Virol. 85:13038-13048. http://dx.doi.org/10.1128/JVI.05834-11.
51. Guo H, Santiago F, Lambert K, Takimoto T, Topham DJ. 2011. T cell-mediated protection against lethal 2009 pandemic H1N1 influenza virus infection in a mouse model. J. Virol. 85:448-455. http://dx.doi.org /10.1128/JVI.01812-10.
52. Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M, Jr, Garcia-Sastre A. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514-524. http://dx.doi.org/10.1128/JVI.01265-06.
53. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
54. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
55. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RA, Pappas C, Alpuche- Aranda CM, Lopez-Gatell H, Olivera H, Lopez I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD, Jr, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197-201. http://dx.doi.org/10 .1126/science.1176225.
56. Wanitchang A, Narkpuk J, Jaru-ampornpan P, Jengarn J, Jongkaewwattana A. 2012. Inhibition of influenza A virus replication by influenza B virus nucleoprotein: an insight into interference between influenza A and B viruses. Virology 432:194-203. http://dx.doi.org/10.1016/j.virol.2012 .06.016.
57. Dos Santos Afonso E, Escriou N, Leclercq I, van der Werf S, Naffakh N. 2005. The generation of recombinant influenza A viruses expressing a PB2 fusion protein requires the conservation of a packaging signal overlapping the coding and noncoding regions at the 5' end of the PB2 segment. Virology 341:34-46. http://dx.doi.org/10.1016/j.virol.2005.06.040.
58. Fujii K, Fujii Y, Noda T, Muramoto Y, Watanabe T, Takada A, Goto H, Horimoto T, Kawaoka Y. 2005. Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J. Virol. 79:3766-3774. http: //dx.doi.org/10.1128/JVI.79.6.3766-3774.2005.
59. Fujii K, Ozawa M, Iwatsuki-Horimoto K, Horimoto T, Kawaoka Y. 2009. Incorporation of influenza A virus genome segments does not absolutely require wild-type sequences. J. Gen. Virol. 90:1734-1740. http: //dx.doi.org/10.1099/vir.0.010355-0.
60. Gog JR, Afonso Edos S, Dalton RM, Leclercq I, Tiley L, Elton D, von Kirchbach JC, Naffakh N, Escriou N, Digard P. 2007. Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res. 35:1897-1907. http://dx.doi.org/10.1093/nar/gkm087.
61. Liang Y, Hong Y, Parslow TG. 2005. cis-Acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J. Virol. 79: 10348-10355. http://dx.doi.org/10.1128/JVI.79.16.10348-10355.2005.
62. Liang Y, Huang T, Ly H, Parslow TG, Liang Y. 2008. Mutational analyses of packaging signals in influenza virus PA, PB1, and PB2 genomic RNA segments. J. Virol. 82:229 -236. http://dx.doi.org/10 .1128/JVI.01541-07.
63. Marsh GA, Rabadan R, Levine AJ, Palese P. 2008. Highly conserved regions of influenza A virus polymerase gene segments are critical for efficient viralRNApackaging. J. Virol. 82:2295-2304. http://dx.doi.org/10 .1128/JVI.02267-07.
64. Muramoto Y, Takada A, Fujii K, Noda T, Iwatsuki-Horimoto K, Watanabe S, Horimoto T, Kida H, Kawaoka Y. 2006. Hierarchy among viral RNA(vRNA) segments in their role in vRNA incorporation into influenza A virions. J. Virol. 80:2318-2325. http://dx.doi.org/10.1128/JVI.80.5 .2318-2325.2006.
65. 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.
66. Ozawa M, Maeda J, Iwatsuki-Horimoto K, Watanabe S, Goto H, Horimoto T, Kawaoka Y. 2009. Nucleotide sequence requirements at the 5= end of the influenza A virusMRNA segment for efficient virus replication. J. Virol. 83:3384-3388. http://dx.doi.org/10.1128/JVI.02513-08.
67. Watanabe T, Watanabe S, Noda T, Fujii Y, Kawaoka Y. 2003. Exploitation of nucleic acid packaging signals to generate a novel influenza virusbased vector stably expressing two foreign genes. J. Virol. 77:10575-10583. http://dx.doi.org/10.1128/JVI.77.19.10575-10583.2003.
68. Pica N, Iyer A, Ramos I, Bouvier NM, Fernandez-Sesma A, Garcia- Sastre A, Lowen AC, Palese P, Steel J. 2011. The DBA.2 mouse is susceptible to disease following infection with a broad, but limited, range of influenza A and B viruses. J. Virol. 85:12825-12829. http://dx.doi.org /10.1128/JVI.05930-11.
69. Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y. 2004. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703-707. http: //dx.doi.org/10.1038/nature02951.
70. Carragher DM, Kaminski DA, Moquin A, Hartson L, Randall TD. 2008. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J. Immunol. 181:4168-4176. http: //dx.doi.org/10.4049/jimmunol.181.6.4168.
71. Dowdle WN, Kendal AP, Noble GR. 1979. Influenza viruses, p 585-609. In Lennette EH, Schmidt NJ (ed), Diagnostic procedures for viral, rickettsial, and chlamydial infections, 5th ed. American Public Health Association, Washington, DC.
72. Jin H, Lu B, Zhou H, Ma C, Zhao J, Yang CF, Kemble G, Greenberg H. 2003. Multiple amino acid residues confer temperature sensitivity to human influenza virus vaccine strains (FluMist) derived from cold-adapted A/Ann Arbor/6/60. Virology 306:18-24. http://dx.doi.org/10.1016/S0042 -6822(02)00035-1.
73. Yewdell JW, Bennink JR, Hosaka Y. 1988. Cells process exogenous proteins for recognition by cytotoxic T lymphocytes. Science 239:637- 640. http://dx.doi.org/10.1126/science.3257585.
74. Suzuki Y, Nei M. 2002. Origin and evolution of influenza virus hemagglutinin genes. Mol. Biol. Evol. 19:501-509. http://dx.doi.org/10.1093 /oxfordjournals.molbev.a004105.
75. Taubenberger JK, Kash JC. 2010. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440-451. http://dx .doi.org/10.1016/j.chom.2010.05.009.
76. Hai R, Garcia-Sastre A, Swayne DE, Palese P. 2011. A reassortmentincompetent live attenuated influenza virus vaccine for protection against pandemic virus strains. J. Virol. 85:6832-6843. http://dx.doi.org/10.1128 /JVI.00609-11.
77. Ali A, Avalos RT, Ponimaskin E, Nayak DP. 2000. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 74:8709-8719. http://dx.doi.org/10.1128 /JVI.74.18.8709-8719.2000.
78. Jambrina E, Barcena J, Uez O, Portela A. 1997. The three subunits of the polymerase and the nucleoprotein of influenza B virus are the minimum set of viral proteins required for expression of a model RNA template. Virology 235:209-217. http://dx.doi.org/10.1006/viro.1997.8682.
79. Fournier E, Moules V, Essere B, Paillart JC, Sirbat JD, Isel C, Cavalier A, Rolland JP, Thomas D, Lina B, Marquet R. 2012. A supramolecular assembly formed by influenza A virus genomic RNA segments. Nucleic Acids Res. 40:2197-2209. http://dx.doi.org/10.1093/nar/gkr985.
80. Essere B, Yver M, Gavazzi C, Terrier O, Isel C, Fournier E, Giroux F, Textoris J, Julien T, Socratous C, Rosa-Calatrava M, Lina B, Marquet R, Moules V. 2013. Critical role of segment-specific packaging signals in genetic reassortment of influenza A viruses. Proc. Natl. Acad. Sci. U. S. A. 110:E3840-E3848. http://dx.doi.org/10.1073/pnas.1308649110.
81. Gavazzi C, Isel C, Fournier E, Moules V, Cavalier A, Thomas D, Lina B, Marquet R. 2013. An in vitro network of intermolecular interactions between viral RNA segments of an avian H5N2 influenza A virus: comparison with a human H3N2 virus. Nucleic Acids Res. 41:1241-1254. http: //dx.doi.org/10.1093/nar/gks1181.
82. Kilbourne ED, Schulman JL, Schild GC, Schloer G, Swanson J, Bucher D. 1971. Related studies of a recombinant influenza-virus vaccine. I. Derivation and characterization of virus and vaccine. J. Infect. Dis. 124:449-462.