1887

Abstract

Influenza A virus (IAV) is an RNA virus with a segmented genome. These viral properties allow for the rapid evolution of IAV under selective pressure, due to mutation occurring from error-prone replication and the exchange of gene segments within a co-infected cell, termed reassortment. Both mutation and reassortment give rise to genetic diversity, but constraints shape their impact on viral evolution: just as most mutations are deleterious, most reassortment events result in genetic incompatibilities. The phenomenon of segment mismatch encompasses both RNA- and protein-based incompatibilities between co-infecting viruses and results in the production of progeny viruses with fitness defects. Segment mismatch is an important determining factor of the outcomes of mixed IAV infections and has been addressed in multiple risk assessment studies undertaken to date. However, due to the complexity of genetic interactions among the eight viral gene segments, our understanding of segment mismatch and its underlying mechanisms remain incomplete. Here, we summarize current knowledge regarding segment mismatch and discuss the implications of this phenomenon for IAV reassortment and diversity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000989
2018-01-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/1/3.html?itemId=/content/journal/jgv/10.1099/jgv.0.000989&mimeType=html&fmt=ahah

References

  1. Shaw ML, Palese P. Orthomyxoviridae. In Knipe D, Howley P. (editors) Fields Virology Philadelphia, PA: Lippincott Williams & Wilkins; 2013; pp.1151–1185
    [Google Scholar]
  2. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA et al. A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 2012;109:4269–4274 [CrossRef][PubMed]
    [Google Scholar]
  3. Tong S, Zhu X, Li Y, Shi M, Zhang J et al. New world bats harbor diverse influenza A viruses. PLoS Pathog 2013;9:e1003657 [CrossRef][PubMed]
    [Google Scholar]
  4. Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A et al. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 2007;3:e61 [CrossRef][PubMed]
    [Google Scholar]
  5. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992;56:152–179[PubMed]
    [Google Scholar]
  6. Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y et al. Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses. PLoS Biol 2005;3:e300 [CrossRef][PubMed]
    [Google Scholar]
  7. Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J et al. Stochastic processes are key determinants of short-term evolution in influenza a virus. PLoS Pathog 2006;2:e125 [CrossRef][PubMed]
    [Google Scholar]
  8. Nelson MI, Edelman L, Spiro DJ, Boyne AR, Bera J et al. Molecular epidemiology of A/H3N2 and A/H1N1 influenza virus during a single epidemic season in the United States. PLoS Pathog 2008;4:e1000133 [CrossRef][PubMed]
    [Google Scholar]
  9. Westgeest KB, Russell CA, Lin X, Spronken MI, Bestebroer TM et al. Genomewide analysis of reassortment and evolution of human influenza A(H3N2) viruses circulating between 1968 and 2011. J Virol 2014;88:2844–2857 [CrossRef][PubMed]
    [Google Scholar]
  10. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK et al. The genomic and epidemiological dynamics of human influenza A virus. Nature 2008;453:615–619 [CrossRef][PubMed]
    [Google Scholar]
  11. Villa M, Lässig M. Fitness cost of reassortment in human influenza. PLoS Pathog 2017;13:e1006685 [CrossRef][PubMed]
    [Google Scholar]
  12. Johnson NP, Mueller J. Updating the accounts: global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull Hist Med 2002;76:105–115 [CrossRef][PubMed]
    [Google Scholar]
  13. Viboud C, Simonsen L, Fuentes R, Flores J, Miller MA et al. Global mortality impact of the 1957-1959 influenza pandemic. J Infect Dis 2016;213:738–745 [CrossRef][PubMed]
    [Google Scholar]
  14. Cockburn WC, Delon PJ, Ferreira W. Origin and progress of the 1968-69 Hong Kong influenza epidemic. Bull World Health Organ 1969;41:345–348[PubMed]
    [Google Scholar]
  15. Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM et al. Global mortality estimates for the 2009 Influenza Pandemic from the GLaMOR project: a modeling study. PLoS Med 2013;10:e1001558 [CrossRef][PubMed]
    [Google Scholar]
  16. Worobey M, Han GZ, Rambaut A. Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus. Proc Natl Acad Sci USA 2014;111:8107–8112 [CrossRef][PubMed]
    [Google Scholar]
  17. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G et al. Characterization of the 1918 influenza virus polymerase genes. Nature 2005;437:889–893 [CrossRef][PubMed]
    [Google Scholar]
  18. Gibbs MJ, Gibbs AJ. Molecular virology: was the 1918 pandemic caused by a bird flu?. Nature 2006;440:E8E8 [CrossRef][PubMed]
    [Google Scholar]
  19. Kilbourne ED. Influenza pandemics of the 20th century. Emerg Infect Dis 2006;12:9–14 [CrossRef][PubMed]
    [Google Scholar]
  20. Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 1989;63:4603–4608[PubMed]
    [Google Scholar]
  21. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009;325:197–201 [CrossRef][PubMed]
    [Google Scholar]
  22. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009;459:1122–1125 [CrossRef][PubMed]
    [Google Scholar]
  23. York I, Donis RO. The 2009 pandemic influenza virus: where did it come from, where is it now, and where is it going?. Curr Top Microbiol Immunol 2013;370:241–257 [CrossRef][PubMed]
    [Google Scholar]
  24. Ku AS, Chan LT. The first case of H5N1 avian influenza infection in a human with complications of adult respiratory distress syndrome and Reye's syndrome. J Paediatr Child Health 1999;35:207–209[PubMed][Crossref]
    [Google Scholar]
  25. Chan PK. Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 2002;34 Suppl 2:S58–S64 [CrossRef][PubMed]
    [Google Scholar]
  26. Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM et al. Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 2004;350:1179–1188 [CrossRef][PubMed]
    [Google Scholar]
  27. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W et al. Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 2005;352:333–340 [CrossRef][PubMed]
    [Google Scholar]
  28. Gao R, Cao B, Hu Y, Feng Z, Wang D et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013;368:1888–1897 [CrossRef][PubMed]
    [Google Scholar]
  29. Fouchier RA, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SA et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA 2004;101:1356–1361 [CrossRef][PubMed]
    [Google Scholar]
  30. WHO 2017; Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2017. www.who.int/influenza/human_animal_interface/2017_09_27_tableH5N1.pdf?ua=1 [accessed 11 November 2017]
  31. WHO 2017; Influenza at the human-animal interface. www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_09_27_2017.pdf?ua=1 [accessed 11 November 2017]
  32. Lam TT, Wang J, Shen Y, Zhou B, Duan L et al. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 2013;502:241–244 [CrossRef][PubMed]
    [Google Scholar]
  33. Wu A, Su C, Wang D, Peng Y, Liu M et al. Sequential reassortments underlie diverse influenza H7N9 genotypes in China. Cell Host Microbe 2013;14:446–452 [CrossRef][PubMed]
    [Google Scholar]
  34. Li KS, Guan Y, Wang J, Smith GJ, Xu KM et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004;430:209–213 [CrossRef][PubMed]
    [Google Scholar]
  35. Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci USA 1999;96:9363–9367 [CrossRef][PubMed]
    [Google Scholar]
  36. Lin YP, Shaw M, Gregory V, Cameron K, Lim W et al. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA 2000;97:9654–9658 [CrossRef][PubMed]
    [Google Scholar]
  37. Chen H, Yuan H, Gao R, Zhang J, Wang D et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 2014;383:714–721 [CrossRef][PubMed]
    [Google Scholar]
  38. Zhang Z, Li R, Jiang L, Xiong C, Chen Y et al. The complexity of human infected AIV H5N6 isolated from China. BMC Infect Dis 2016;16:600 [CrossRef][PubMed]
    [Google Scholar]
  39. Huang Y, Li X, Zhang H, Chen B, Jiang Y et al. Human infection with an avian influenza A (H9N2) virus in the middle region of China. J Med Virol 2015;87:1641–1648 [CrossRef][PubMed]
    [Google Scholar]
  40. Yuan J, Zhang L, Kan X, Jiang L, Yang J et al. Origin and molecular characteristics of a novel 2013 avian influenza A(H6N1) virus causing human infection in Taiwan. Clin Infect Dis 2013;57:1367–1368 [CrossRef][PubMed]
    [Google Scholar]
  41. Lubeck MD, Palese P, Schulman JL. Nonrandom association of parental genes in influenza A virus recombinants. Virology 1979;95:269–274 [CrossRef][PubMed]
    [Google Scholar]
  42. Greenbaum BD, Li OT, Poon LL, Levine AJ, Rabadan R. Viral reassortment as an information exchange between viral segments. Proc Natl Acad Sci USA 2012;109:3341–3346 [CrossRef][PubMed]
    [Google Scholar]
  43. Pauly MD, Procario MC, Lauring AS. A novel twelve class fluctuation test reveals higher than expected mutation rates for influenza A viruses. eLife 2017;6: [CrossRef][PubMed]
    [Google Scholar]
  44. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 2011;208:181–193 [CrossRef][PubMed]
    [Google Scholar]
  45. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M et al. Antibody recognition of a highly conserved influenza virus epitope. Science 2009;324:246–251 [CrossRef][PubMed]
    [Google Scholar]
  46. Memoli MJ, Shaw PA, Han A, Czajkowski L, Reed S et al. Evaluation of antihemagglutinin and antineuraminidase antibodies as correlates of protection in an influenza A/H1N1 virus healthy human challenge model. MBio 2016;7:e00417-16 [CrossRef][PubMed]
    [Google Scholar]
  47. Gerhard W, Yewdell J, Frankel ME, Webster R. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 1981;290:713–717 [CrossRef][PubMed]
    [Google Scholar]
  48. Plotkin JB, Dushoff J, Levin SA. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc Natl Acad Sci USA 2002;99:6263–6268 [CrossRef][PubMed]
    [Google Scholar]
  49. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF et al. Mapping the antigenic and genetic evolution of influenza virus. Science 2004;305:371–376 [CrossRef][PubMed]
    [Google Scholar]
  50. Cox NJ, Brammer TL, Regnery HL. Influenza: global surveillance for epidemic and pandemic variants. Eur J Epidemiol 1994;10:467–470 [CrossRef][PubMed]
    [Google Scholar]
  51. Nelson MI, Viboud C, Simonsen L, Bennett RT, Griesemer SB et al. Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 2008;4:e1000012 [CrossRef][PubMed]
    [Google Scholar]
  52. Nelson MI, Holmes EC. The evolution of epidemic influenza. Nat Rev Genet 2007;8:196–205 [CrossRef][PubMed]
    [Google Scholar]
  53. Simonsen L, Viboud C, Grenfell BT, Dushoff J, Jennings L et al. The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol 2007;24:1811–1820 [CrossRef][PubMed]
    [Google Scholar]
  54. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC. The origin and global emergence of adamantane resistant A/H3N2 influenza viruses. Virology 2009;388:270–278 [CrossRef][PubMed]
    [Google Scholar]
  55. Wright P, Neumann G, Kawaoka Y. Orthomyxoviruses. In Knipe D, Howley P. (editors) Fields Virology Philadelphia, PA: Lippincott Williams & Wilkins; 2013
    [Google Scholar]
  56. Ellis JS, Alvarez-Aguero A, Gregory V, Lin YP, Hay A et al. Influenza AH1N2 viruses, United Kingdom, 2001-02 influenza season. Emerg Infect Dis 2003;9:304–310 [CrossRef][PubMed]
    [Google Scholar]
  57. Chen MJ, La T, Zhao P, Tam JS, Rappaport R et al. Genetic and phylogenetic analysis of multi-continent human influenza A(H1N2) reassortant viruses isolated in 2001 through 2003. Virus Res 2006;122:200–205 [CrossRef][PubMed]
    [Google Scholar]
  58. Gregory V, Bennett M, Orkhan MH, Al Hajjar S, Varsano N et al. Emergence of influenza A H1N2 reassortant viruses in the human population during 2001. Virology 2002;300:1–7 [CrossRef][PubMed]
    [Google Scholar]
  59. Xu X, Smith CB, Mungall BA, Lindstrom SE, Hall HE et al. Intercontinental circulation of human influenza A(H1N2) reassortant viruses during the 2001-2002 influenza season. J Infect Dis 2002;186:1490–1493 [CrossRef][PubMed]
    [Google Scholar]
  60. Mukherjee TR, Agrawal AS, Chakrabarti S, Chawla-Sarkar M. Full genomic analysis of an influenza A (H1N2) virus identified during 2009 pandemic in Eastern India: evidence of reassortment event between co-circulating A(H1N1)pdm09 and A/Brisbane/10/2007-like H3N2 strains. Virol J 2012;9:1–10 [CrossRef]
    [Google Scholar]
  61. Rith S, Chin S, Sar B, Phalla Y, Horm SV et al. Natural co-infection of influenza A/H3N2 and A/H1N1pdm09 viruses resulting in a reassortant A/H3N2 virus. J Clin Virol 2015;73:108–111 [CrossRef][PubMed]
    [Google Scholar]
  62. Liu W, Li ZD, Tang F, Wei MT, Tong YG et al. Mixed infections of pandemic H1N1 and seasonal H3N2 viruses in 1 outbreak. Clin Infect Dis 2010;50:1359–1365 [CrossRef][PubMed]
    [Google Scholar]
  63. Myers CA, Kasper MR, Yasuda CY, Savuth C, Spiro DJ et al. Dual infection of novel influenza viruses A/H1N1 and A/H3N2 in a cluster of Cambodian patients. Am J Trop Med Hyg 2011;85:961–963 [CrossRef][PubMed]
    [Google Scholar]
  64. Yamane N, Arikawa J, Odagiri T, Sukeno N, Ishida N. Isolation of three different influenza A viruses from an individual after probable double infection with H3N2 and H1N1 viruses. Jpn J Med Sci Biol 1978;31:431–434 [CrossRef][PubMed]
    [Google Scholar]
  65. Falchi A, Arena C, Andreoletti L, Jacques J, Leveque N et al. Dual infections by influenza A/H3N2 and B viruses and by influenza A/H3N2 and A/H1N1 viruses during winter 2007, Corsica Island, France. J Clin Virol 2008;41:148–151 [CrossRef][PubMed]
    [Google Scholar]
  66. Kendal AP, Lee DT, Parish HS, Raines D, Noble GR et al. Laboratory-based surveillance of influenza virus in the United States during the winter of 1977-1978. II. Isolation of a mixture of A/Victoria- and A/USSR-like viruses from a single person during an epidemic in Wyoming, USA, January 1978. Am J Epidemiol 1979;110:462–468[PubMed][Crossref]
    [Google Scholar]
  67. Frank AL, Taber LH, Wells JM. Individuals infected with two subtypes of influenza A virus in the same season. J Infect Dis 1983;147:120–124 [CrossRef][PubMed]
    [Google Scholar]
  68. Nishikawa F, Sugiyama T. Direct isolation of H1N2 recombinant virus from a throat swab of a patient simultaneously infected with H1N1 and H3N2 influenza A viruses. J Clin Microbiol 1983;18:425–427[PubMed]
    [Google Scholar]
  69. Phipps KL, Marshall N, Tao H, Danzy S, Onuoha N et al. Seasonal H3N2 and 2009 pandemic H1N1 influenza A viruses reassort efficiently but produce attenuated progeny. J Virol 2017;91:e00830-17 [CrossRef][PubMed]
    [Google Scholar]
  70. Schrauwen EJ, Herfst S, Chutinimitkul S, Bestebroer TM, Rimmelzwaan GF et al. Possible increased pathogenicity of pandemic (H1N1) 2009 influenza virus upon reassortment. Emerg Infect Dis 2011;17:200–208 [CrossRef][PubMed]
    [Google Scholar]
  71. Mena I, Nelson MI, Quezada-Monroy F, Dutta J, Cortes-Fernández R et al. Origins of the 2009 H1N1 influenza pandemic in swine in Mexico. eLife 2016;5: [CrossRef][PubMed]
    [Google Scholar]
  72. Ma W, Liu Q, Qiao C, del Real G, García-Sastre A et al. North American triple reassortant and Eurasian H1N1 swine influenza viruses do not readily reassort to generate a 2009 pandemic H1N1-like virus. mBio 2014;5:e00919-13 [CrossRef][PubMed]
    [Google Scholar]
  73. Kaverin NV, Gambaryan AS, Bovin NV, Rudneva IA, Shilov AA et al. Postreassortment changes in influenza A virus hemagglutinin restoring HA-NA functional match. Virology 1998;244:315–321 [CrossRef][PubMed]
    [Google Scholar]
  74. Ilyushina NA, Rudneva IA, Shilov AA, Klenk HD, Kaverin NV. Postreassortment changes in a model system: HA-NA adjustment in an H3N2 avian-human reassortant influenza virus. Arch Virol 2005;150:1327–1338 [CrossRef][PubMed]
    [Google Scholar]
  75. Neverov AD, Lezhnina KV, Kondrashov AS, Bazykin GA. Intrasubtype reassortments cause adaptive amino acid replacements in H3N2 influenza genes. PLoS Genet 2014;10:e1004037 [CrossRef][PubMed]
    [Google Scholar]
  76. Steel J, Lowen AC. Influenza A virus reassortment. Curr Top Microbiol Immunol 2014;385:377–401 [CrossRef][PubMed]
    [Google Scholar]
  77. Marshall N, Priyamvada L, Ende Z, Steel J, Lowen AC. Influenza virus reassortment occurs with high frequency in the absence of segment mismatch. PLoS Pathog 2013;9:e1003421 [CrossRef][PubMed]
    [Google Scholar]
  78. Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ. High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 2003;49:853–860 [CrossRef][PubMed]
    [Google Scholar]
  79. Fonville JM, Marshall N, Tao H, Steel J, Lowen AC. Influenza virus reassortment is enhanced by semi-infectious particles but can be suppressed by defective interfering particles. PLoS Pathog 2015;11:e1005204 [CrossRef][PubMed]
    [Google Scholar]
  80. Huang IC, Li W, Sui J, Marasco W, Choe H et al. Influenza A virus neuraminidase limits viral superinfection. J Virol 2008;82:4834–4843 [CrossRef][PubMed]
    [Google Scholar]
  81. Tao H, Steel J, Lowen AC. Intrahost dynamics of influenza virus reassortment. J Virol 2014;88:7485–7492 [CrossRef][PubMed]
    [Google Scholar]
  82. Tao H, Li L, White MC, Steel J, Lowen AC. Influenza A virus coinfection through transmission can support high levels of reassortment. J Virol 2015;89:8453–8461 [CrossRef][PubMed]
    [Google Scholar]
  83. Wille M, Tolf C, Avril A, Latorre-Margalef N, Wallerström S et al. Frequency and patterns of reassortment in natural influenza A virus infection in a reservoir host. Virology 2013;443:150–160 [CrossRef][PubMed]
    [Google Scholar]
  84. Deng G, Tan D, Shi J, Cui P, Jiang Y et al. Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the Dongting Lake Region of China. J Virol 2013;87:9452–9462 [CrossRef][PubMed]
    [Google Scholar]
  85. Abolnik C, Gerdes GH, Sinclair M, Ganzevoort BW, Kitching JP et al. Phylogenetic analysis of influenza A viruses (H6N8, H1N8, H4N2, H9N2, H10N7) isolated from wild birds, ducks, and ostriches in South Africa from 2007 to 2009. Avian Dis 2010;54:313–322 [CrossRef][PubMed]
    [Google Scholar]
  86. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J et al. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 2008;4:e1000076 [CrossRef][PubMed]
    [Google Scholar]
  87. Nelson MI, Detmer SE, Wentworth DE, Tan Y, Schwartzbard A et al. Genomic reassortment of influenza A virus in North American swine, 1998-2011. J Gen Virol 2012;93:2584–2589 [CrossRef][PubMed]
    [Google Scholar]
  88. Vijaykrishna D, Poon LL, Zhu HC, Ma SK, Li OT et al. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 2010;328:1529 [CrossRef][PubMed]
    [Google Scholar]
  89. Rabadan R, Levine AJ, Krasnitz M. Non-random reassortment in human influenza A viruses. Influenza Other Respir Viruses 2008;2:9–22 [CrossRef][PubMed]
    [Google Scholar]
  90. Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T et al. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci USA 2006;103:12121–12126 [CrossRef][PubMed]
    [Google Scholar]
  91. Jackson S, van Hoeven N, Chen LM, Maines TR, Cox NJ et al. Reassortment between avian H5N1 and human H3N2 influenza viruses in ferrets: a public health risk assessment. J Virol 2009;83:8131–8140 [CrossRef][PubMed]
    [Google Scholar]
  92. Chen LM, Davis CT, Zhou H, Cox NJ, Donis RO. Genetic compatibility and virulence of reassortants derived from contemporary avian H5N1 and human H3N2 influenza A viruses. PLoS Pathog 2008;4:e1000072 [CrossRef][PubMed]
    [Google Scholar]
  93. Schrauwen EJ, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA et al. Reassortment between Avian H5N1 and human influenza viruses is mainly restricted to the matrix and neuraminidase gene segments. PLoS One 2013;8:e59889 [CrossRef][PubMed]
    [Google Scholar]
  94. Kimble JB, Sorrell E, Shao H, Martin PL, Perez DR. Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci USA 2011;108:12084–12088 [CrossRef][PubMed]
    [Google Scholar]
  95. Dlugolenski D, Jones L, Howerth E, Wentworth D, Tompkins SM et al. Swine influenza virus PA and neuraminidase gene reassortment into human H1N1 influenza virus is associated with an altered pathogenic phenotype linked to increased MIP-2 expression. J Virol 2015;89:5651–5667 [CrossRef][PubMed]
    [Google Scholar]
  96. Ma J, Shen H, Liu Q, Bawa B, Qi W et al. Pathogenicity and transmissibility of novel reassortant H3N2 influenza viruses with 2009 pandemic H1N1 genes in pigs. J Virol 2015;89:2831–2841 [CrossRef][PubMed]
    [Google Scholar]
  97. Enami M, Sharma G, Benham C, Palese P. An influenza virus containing nine different RNA segments. Virology 1991;185:291–298 [CrossRef][PubMed]
    [Google Scholar]
  98. Donald HB, Isaacs A. Counts of influenza virus particles. J Gen Microbiol 1954;10:457–464 [CrossRef][PubMed]
    [Google Scholar]
  99. Mclain L, Armstrong SJ, Dimmock NJ. One defective interfering particle per cell prevents influenza virus-mediated cytopathology: an efficient assay system. J Gen Virol 1988;69:1415–1419 [CrossRef][PubMed]
    [Google Scholar]
  100. Isaacs A, Donald HB. Particle counts of haemagglutinating viruses. J Gen Microbiol 1955;12:241–247 [CrossRef][PubMed]
    [Google Scholar]
  101. Bancroft CT, Parslow TG. Evidence for segment-nonspecific packaging of the influenza a virus genome. J Virol 2002;76:7133–7139 [CrossRef][PubMed]
    [Google Scholar]
  102. Gerber M, Isel C, Moules V, Marquet R. Selective packaging of the influenza A genome and consequences for genetic reassortment. Trends Microbiol 2014;22:446–455 [CrossRef][PubMed]
    [Google Scholar]
  103. Mcgeoch D, Fellner P, Newton C. Influenza virus genome consists of eight distinct RNA species. Proc Natl Acad Sci USA 1976;73:3045–3049 [CrossRef][PubMed]
    [Google Scholar]
  104. Nakajima K, Sugiura A. Three-factor cross of influenza virus. Virology 1977;81:486–489 [CrossRef][PubMed]
    [Google Scholar]
  105. Bergmann M, Muster T. The relative amount of an influenza A virus segment present in the viral particle is not affected by a reduction in replication of that segment. J Gen Virol 1995;76:3211–3215 [CrossRef][PubMed]
    [Google Scholar]
  106. Smith GL, Hay AJ. Replication of the influenza virus genome. Virology 1982;118:96–108 [CrossRef][PubMed]
    [Google Scholar]
  107. Chou YY, Vafabakhsh R, Doğanay S, Gao Q, Ha T et al. One influenza virus particle packages eight unique viral RNAs as shown by FISH analysis. Proc Natl Acad Sci USA 2012;109:9101–9106 [CrossRef][PubMed]
    [Google Scholar]
  108. Inagaki A, Goto H, Kakugawa S, Ozawa M, Kawaoka Y. Competitive incorporation of homologous gene segments of influenza A virus into virions. J Virol 2012;86:10200–10202 [CrossRef][PubMed]
    [Google Scholar]
  109. Duhaut SD, Dimmock NJ. Defective segment 1 RNAs that interfere with production of infectious influenza A virus require at least 150 nucleotides of 5' sequence: evidence from a plasmid-driven system. J Gen Virol 2002;83:403–411 [CrossRef][PubMed]
    [Google Scholar]
  110. Duhaut SD, Mccauley JW. Defective RNAs inhibit the assembly of influenza virus genome segments in a segment-specific manner. Virology 1996;216:326–337 [CrossRef][PubMed]
    [Google Scholar]
  111. Odagiri T, Tashiro M. Segment-specific noncoding sequences of the influenza virus genome RNA are involved in the specific competition between defective interfering RNA and its progenitor RNA segment at the virion assembly step. J Virol 1997;71:2138–2145[PubMed]
    [Google Scholar]
  112. Odagiri T, Tominaga K, Tobita K, Ohta S. An amino acid change in the non-structural NS2 protein of an influenza A virus mutant is responsible for the generation of defective interfering (DI) particles by amplifying DI RNAs and suppressing complementary RNA synthesis. J Gen Virol 1994;75:43–53 [CrossRef][PubMed]
    [Google Scholar]
  113. Fujii Y, Goto H, Watanabe T, Yoshida T, Kawaoka Y. Selective incorporation of influenza virus RNA segments into virions. Proc Natl Acad Sci USA 2003;100:2002–2007 [CrossRef][PubMed]
    [Google Scholar]
  114. Liang Y, Hong Y, Parslow TG. cis-Acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J Virol 2005;79:10348–10355 [CrossRef][PubMed]
    [Google Scholar]
  115. Watanabe T, Watanabe S, Noda T, Fujii Y, Kawaoka Y. Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J Virol 2003;77:10575–10583 [CrossRef][PubMed]
    [Google Scholar]
  116. Ozawa M, Fujii K, Muramoto Y, Yamada S, Yamayoshi S et al. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J Virol 2007;81:30–41 [CrossRef][PubMed]
    [Google Scholar]
  117. Ozawa M, Maeda J, Iwatsuki-Horimoto K, Watanabe S, Goto H et al. Nucleotide sequence requirements at the 5' end of the influenza A virus M RNA segment for efficient virus replication. J Virol 2009;83:3384–3388 [CrossRef][PubMed]
    [Google Scholar]
  118. Fujii K, Fujii Y, Noda T, Muramoto Y, Watanabe T et al. 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 2005;79:3766–3774 [CrossRef][PubMed]
    [Google Scholar]
  119. Cobbin JC, Ong C, Verity E, Gilbertson BP, Rockman SP et al. Influenza virus PB1 and neuraminidase gene segments can cosegregate during vaccine reassortment driven by interactions in the PB1 coding region. J Virol 2014;88:8971–8980 [CrossRef][PubMed]
    [Google Scholar]
  120. Gilbertson B, Zheng T, Gerber M, Printz-Schweigert A, Ong C et al. Influenza NA and PB1 gene segments interact during the formation of viral progeny: localization of the binding region within the PB1 Gene. Viruses 2016;8:238 [CrossRef][PubMed]
    [Google Scholar]
  121. Gavazzi C, Yver M, Isel C, Smyth RP, Rosa-Calatrava M et al. A functional sequence-specific interaction between influenza A virus genomic RNA segments. Proc Natl Acad Sci USA 2013;110:16604–16609 [CrossRef][PubMed]
    [Google Scholar]
  122. Moreira ÉA, Weber A, Bolte H, Kolesnikova L, Giese S et al. A conserved influenza A virus nucleoprotein code controls specific viral genome packaging. Nat Commun 2016;7:12861 [CrossRef][PubMed]
    [Google Scholar]
  123. Noda T, Sagara H, Yen A, Takada A, Kida H et al. Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 2006;439:490–492 [CrossRef][PubMed]
    [Google Scholar]
  124. Nakatsu S, Sagara H, Sakai-Tagawa Y, Sugaya N, Noda T et al. Complete and Incomplete genome packaging of influenza A and B viruses. mBio 2016;7:e01248-16 [CrossRef][PubMed]
    [Google Scholar]
  125. Noda T, Sugita Y, Aoyama K, Hirase A, Kawakami E et al. Three-dimensional analysis of ribonucleoprotein complexes in influenza A virus. Nat Commun 2012;3:639 [CrossRef][PubMed]
    [Google Scholar]
  126. Fournier E, Moules V, Essere B, Paillart JC, Sirbat JD et al. Interaction network linking the human H3N2 influenza A virus genomic RNA segments. Vaccine 2012;30:7359–7367 [CrossRef][PubMed]
    [Google Scholar]
  127. White MC, Steel J, Lowen AC. Heterologous packaging signals on segment 4, but not segment 6 or segment 8, limit influenza A virus reassortment. J Virol 2017;91:e00195-17 [CrossRef][PubMed]
    [Google Scholar]
  128. Baker SF, Nogales A, Finch C, Tuffy KM, Domm W et al. Influenza A and B virus intertypic reassortment through compatible viral packaging signals. J Virol 2014;88:10778–10791 [CrossRef][PubMed]
    [Google Scholar]
  129. Essere B, Yver M, Gavazzi C, Terrier O, Isel C et al. Critical role of segment-specific packaging signals in genetic reassortment of influenza A viruses. Proc Natl Acad Sci USA 2013;110:E3840E3848 [CrossRef][PubMed]
    [Google Scholar]
  130. Gao Q, Palese P. Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci USA 2009;106:15891–15896 [CrossRef][PubMed]
    [Google Scholar]
  131. Li C, Hatta M, Watanabe S, Neumann G, Kawaoka Y. Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J Virol 2008;82:11880–11888 [CrossRef][PubMed]
    [Google Scholar]
  132. Hatta M, Halfmann P, Wells K, Kawaoka Y. Human influenza a viral genes responsible for the restriction of its replication in duck intestine. Virology 2002;295:250–255 [CrossRef][PubMed]
    [Google Scholar]
  133. Song MS, Pascua PN, Lee JH, Baek YH, Park KJ et al. Virulence and genetic compatibility of polymerase reassortant viruses derived from the pandemic (H1N1) 2009 influenza virus and circulating influenza A viruses. J Virol 2011;85:6275–6286 [CrossRef][PubMed]
    [Google Scholar]
  134. Octaviani CP, Goto H, Kawaoka Y. Reassortment between seasonal H1N1 and pandemic (H1N1) 2009 influenza viruses is restricted by limited compatibility among polymerase subunits. J Virol 2011;85:8449–8452 [CrossRef][PubMed]
    [Google Scholar]
  135. Hara K, Nakazono Y, Kashiwagi T, Hamada N, Watanabe H. Co-incorporation of the PB2 and PA polymerase subunits from human H3N2 influenza virus is a critical determinant of the replication of reassortant ribonucleoprotein complexes. J Gen Virol 2013;94:2406–2416 [CrossRef][PubMed]
    [Google Scholar]
  136. Wagner R, Matrosovich M, Klenk HD. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 2002;12:159–166 [CrossRef][PubMed]
    [Google Scholar]
  137. Rudneva IA, Kovaleva VP, Varich NL, Farashyan VR, Gubareva LV et al. Influenza A virus reassortants with surface glycoprotein genes of the avian parent viruses: effects of HA and NA gene combinations on virus aggregation. Arch Virol 1993;133:437–450 [CrossRef][PubMed]
    [Google Scholar]
  138. Rudneva IA, Sklyanskaya EI, Barulina OS, Yamnikova SS, Kovaleva VP et al. Phenotypic expression of HA-NA combinations in human-avian influenza A virus reassortants. Arch Virol 1996;141:1091–1099 [CrossRef][PubMed]
    [Google Scholar]
  139. Castrucci MR, Kawaoka Y. Biologic importance of neuraminidase stalk length in influenza A virus. J Virol 1993;67:759–764[PubMed]
    [Google Scholar]
  140. Mitnaul LJ, Matrosovich MN, Castrucci MR, Tuzikov AB, Bovin NV et al. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J Virol 2000;74:6015–6020 [CrossRef][PubMed]
    [Google Scholar]
  141. García-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE et al. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 1998;252:324–330 [CrossRef][PubMed]
    [Google Scholar]
  142. O'Neill RE, Talon J, Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. Embo J 1998;17:288–296 [CrossRef][PubMed]
    [Google Scholar]
  143. Robb NC, Smith M, Vreede FT, Fodor E. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J Gen Virol 2009;90:1398–1407 [CrossRef][PubMed]
    [Google Scholar]
  144. Marión RM, Zürcher T, de La Luna S, Ortín J. Influenza virus NS1 protein interacts with viral transcription-replication complexes in vivo. J Gen Virol 1997;78:2447–2451 [CrossRef][PubMed]
    [Google Scholar]
  145. Robb NC, Chase G, Bier K, Vreede FT, Shaw PC et al. The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. J Virol 2011;85:5228–5231 [CrossRef][PubMed]
    [Google Scholar]
  146. Min JY, Li S, Sen GC, Krug RM. A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology 2007;363:236–243 [CrossRef][PubMed]
    [Google Scholar]
  147. de La Luna S, Fortes P, Beloso A, Ortín J. Influenza virus NS1 protein enhances the rate of translation initiation of viral mRNAs. J Virol 1995;69:2427–2433[PubMed]
    [Google Scholar]
  148. Enami K, Sato TA, Nakada S, Enami M. Influenza virus NS1 protein stimulates translation of the M1 protein. J Virol 1994;68:1432–1437[PubMed]
    [Google Scholar]
  149. Falcón AM, Marión RM, Zürcher T, Gómez P, Portela A et al. Defective RNA replication and late gene expression in temperature-sensitive influenza viruses expressing deleted forms of the NS1 protein. J Virol 2004;78:3880–3888 [CrossRef][PubMed]
    [Google Scholar]
  150. Wang Z, Robb NC, Lenz E, Wolff T, Fodor E et al. NS reassortment of an H7-type highly pathogenic avian influenza virus affects its propagation by altering the regulation of viral RNA production and antiviral host response. J Virol 2010;84:11323–11335 [CrossRef][PubMed]
    [Google Scholar]
  151. Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3'end formation of cellular pre-mRNAs. Mol Cell 1998;1:991–1000 [CrossRef][PubMed]
    [Google Scholar]
  152. Hale BG, Steel J, Medina RA, Manicassamy B, Ye J et al. Inefficient control of host gene expression by the 2009 pandemic H1N1 influenza A virus NS1 protein. J Virol 2010;84:6909–6922 [CrossRef][PubMed]
    [Google Scholar]
  153. Ayllon J, Domingues P, Rajsbaum R, Miorin L, Schmolke M et al. A single amino acid substitution in the novel H7N9 influenza A virus NS1 protein increases CPSF30 binding and virulence. J Virol 2014;88:12146–12151 [CrossRef][PubMed]
    [Google Scholar]
  154. Kuo RL, Krug RM. Influenza a virus polymerase is an integral component of the CPSF30-NS1A protein complex in infected cells. J Virol 2009;83:1611–1616 [CrossRef][PubMed]
    [Google Scholar]
  155. Twu KY, Kuo RL, Marklund J, Krug RM. The H5N1 influenza virus NS genes selected after 1998 enhance virus replication in mammalian cells. J Virol 2007;81:8112–8121 [CrossRef][PubMed]
    [Google Scholar]
  156. Shelton H, Smith M, Hartgroves L, Stilwell P, Roberts K et al. An influenza reassortant with polymerase of pH1N1 and NS gene of H3N2 influenza A virus is attenuated in vivo. J Gen Virol 2012;93:998–1006 [CrossRef][PubMed]
    [Google Scholar]
  157. Ince WL, Gueye-Mbaye A, Bennink JR, Yewdell JW. Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host. J Virol 2013;87:4330–4338 [CrossRef][PubMed]
    [Google Scholar]
  158. Ma EJ, Hill NJ, Zabilansky J, Yuan K, Runstadler JA. Reticulate evolution is favored in influenza niche switching. Proc Natl Acad Sci USA 2016;113:5335–5339 [CrossRef][PubMed]
    [Google Scholar]
  159. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S et al. Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proc Natl Acad Sci USA 2010;107:4687–4692 [CrossRef][PubMed]
    [Google Scholar]
  160. Octaviani CP, Ozawa M, Yamada S, Goto H, Kawaoka Y. High level of genetic compatibility between swine-origin H1N1 and highly pathogenic avian H5N1 influenza viruses. J Virol 2010;84:10918–10922 [CrossRef][PubMed]
    [Google Scholar]
  161. Stincarelli M, Arvia R, de Marco MA, Clausi V, Corcioli F et al. Reassortment ability of the 2009 pandemic H1N1 influenza virus with circulating human and avian influenza viruses: public health risk implications. Virus Res 2013;175:151–154 [CrossRef][PubMed]
    [Google Scholar]
  162. Octaviani CP, Li C, Noda T, Kawaoka Y. Reassortment between seasonal and swine-origin H1N1 influenza viruses generates viruses with enhanced growth capability in cell culture. Virus Res 2011;156:147–150 [CrossRef][PubMed]
    [Google Scholar]
  163. Fabrizio TP, Sun Y, Yoon SW, Jeevan T, Dlugolenski D et al. Virologic differences do not fully explain the diversification of swine influenza viruses in the United States. J Virol 2016;90:10074–10082 [CrossRef][PubMed]
    [Google Scholar]
  164. Hao X, Hu J, Wang J, Xu J, Cheng H et al. Reassortant H5N1 avian influenza viruses containing PA or NP gene from an H9N2 virus significantly increase the pathogenicity in mice. Vet Microbiol 2016;192:95–101 [CrossRef][PubMed]
    [Google Scholar]
  165. Ma W, Brenner D, Wang Z, Dauber B, Ehrhardt C et al. The NS segment of an H5N1 highly pathogenic avian influenza virus (HPAIV) is sufficient to alter replication efficiency, cell tropism, and host range of an H7N1 HPAIV. J Virol 2010;84:2122–2133 [CrossRef][PubMed]
    [Google Scholar]
  166. Cline TD, Karlsson EA, Freiden P, Seufzer BJ, Rehg JE et al. Increased pathogenicity of a reassortant 2009 pandemic H1N1 influenza virus containing an H5N1 hemagglutinin. J Virol 2011;85:12262–12270 [CrossRef][PubMed]
    [Google Scholar]
  167. Zhang Y, Zhang Q, Kong H, Jiang Y, Gao Y et al. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 2013;340:1459–1463 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000989
Loading
/content/journal/jgv/10.1099/jgv.0.000989
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error