Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host

Journal of Virology

Volumn 87, Issue 8, 2013, Pages 4330-4338

  Ince, William L ^a   Gueye Mbaye, Aissatou ^a   Bennink, Jack R ^a   Yewdell, Jonathan W ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC REASSORTMENT; GUINEA PIG; INFLUENZA VIRUS A; M1 GENE; MUTATIONAL ANALYSIS; MUTATOR GENE; NONHUMAN; NP GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS GENOME; VIRUS MUTATION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ADAPTATION, BIOLOGICAL; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GUINEA PIGS; INFLUENZA A VIRUS; MICE; MUTATION, MISSENSE; NASAL CAVITY; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINATION, GENETIC; RNA-BINDING PROTEINS; SERIAL PASSAGE; VIRAL CORE PROTEINS; VIRAL MATRIX PROTEINS;

AVES; CAVIA; INFLUENZA A VIRUS; MAMMALIA; MUS;

EID: 84875796093     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02749-12     Document Type: Article

References (40)

1. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK. 2008. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 4:e1000076. doi:10.1371/journal.ppat.1000076.
2. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA. 2006. Global patterns of influenza A virus in wild birds. Science 312:384-388.
3. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179. 4. Brown IH. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74:29-46.
4. Brown IH. 2000. The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74:29-46.
5. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122-1125.
6. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, Dunfee RL, Schwartzman LM, Ozinsky A, Bell GL, Dalton RM, Lo A, Efstathiou S, Atkins JF, Firth AE, Taubenberger JK, Digard P. 2012. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337:199-204.
7. Palese P, Shaw M. 2007. Orthomyxoviridae: the viruses and their replication, p 1647-1689. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
8. Suárez P, Valcarcel J, Ortin J. 1992. Heterogeneity of the mutation rates of influenza A viruses: isolation of mutator mutants. J. Virol. 66:2491-2494.
9. Medina RA, Garcia-Sastre A. 2011. Influenza A viruses: new research developments. Nat. Rev. Microbiol. 9:590-603.
10. Barnard DL. 2009. Animal models for the study of influenza pathogenesis and therapy. Antiviral Res. 82:A110-A122. doi:10.1016/j.antiviral.2008 .12.014.
11. Bouvier NM, Lowen AC. 2010. Animal models for influenza virus pathogenesis and transmission. Viruses 2:1530-1563.
12. O'Donnell CD, Subbarao K. 2011. The contribution of animal models to the understanding of the host range and virulence of influenza A viruses. Microbes Infect. 13:502-515.
13. Bouvier NM, Lowen AC, Palese P. 2008. Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J. Virol. 82:10052-10058.
14. Lowen AC, Mubareka S, Tumpey TM, Garcia-Sastre A, Palese P. 2006. The guinea pig as a transmission model for human influenza viruses. Proc. Natl. Acad. Sci. U. S. A. 103:9988-9992.
15. Lowen AC, Steel J, Mubareka S, Carnero E, Garcia-Sastre A, Palese P. 2009. Blocking interhost transmission of influenza virus by vaccination in the guinea pig model. J. Virol. 83:2803-2818.
16. Martinez-Sobrido L, Garcia-Sastre A. 2010. Generation of recombinant influenza virus from plasmid DNA. J. Vis. Exp. 42:e2057. doi:10.3791 /2057.
17. Vallejo AN, Pogulis RJ, Pease LR. 2008. PCR mutagenesis by overlap extension and gene SOE. CSH Protoc. 2008:pdb.prot4861. doi:10.1101 /pdb.prot4861.
18. Szretter KJ, Balish AL, Katz JM. 2006. Influenza: propagation, quantification, and storage. Curr. Protoc. Microbiol. 3:15G.1.1-15G.1.22. doi:10 .1002/0471729256.mc15g01s3.
19. Zhou B, Wentworth DE. 2012. Influenza A virus molecular virology techniques. Methods Mol. Biol. 865:175-192.
20. Gerber P, Loosli CG, Hambre D. 1955. Antigenic variants of influenza A virus, PR8 strain. I. Their development during serial passage in the lungs of partially immune mice. J. Exp. Med. 101:627-638.
21. Quilligan JJ, Jr, Minuse E, Francis T, Jr. 1948. Homologous and heterologous antibody response of infants and children to multiple injections of a single strain of influenza virus. J. Clin. Invest. 27:572-579.
22. Chou YY, Albrecht RA, Pica N, Lowen AC, Richt JA, Garcia-Sastre A, Palese P, Hai R. 2011. The M segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the guinea pig model. J. Virol. 85:11235-11241.
23. Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, Lowen AC. 2010. Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J. Virol. 84:21-26.
24. Sun Y, Bi Y, Pu J, Hu Y, Wang J, Gao H, Liu L, Xu Q, Tan Y, Liu M, Guo X, Yang H, Liu J. 2010. Guinea pig model for evaluating the potential public health risk of swine and avian influenza viruses. PLoS One 5:e15537. doi:10.1371/journal.pone.0015537.
25. Hanley JA, Lippman-Hand A. 1983. If nothing goes wrong, is everything all right? Interpreting zero numerators. JAMA 249:1743-1745.
26. Centers for Disease Control and Prevention. 2012. Update: influenza A (H3N2)v transmission and guidelines-five states, 2011. MMWR Morb. Mortal. Wkly. Rep. 60:1741-1744.
27. Biswas SK, Boutz PL, Nayak DP. 1998. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. J. Virol. 72:5493-5501.
28. Leyva-Grado VH, Mubareka S, Krammer F, Cárdenas WB, Palese P. 2012. Influenza virus infection in guinea pigs raised as livestock, Ecuador. Emerg. Infect. Dis. doi:10.3201/eid1807.111930.
29. Reperant LA, Kuiken T, Osterhaus AD. 2012. Adaptive pathways of zoonotic influenza viruses: from exposure to establishment in humans. Vaccine 30:4419-4434.
30. Gabriel G, Herwig A, Klenk HD. 2008. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 4:e11. doi:10.1371/journal.ppat.0040011.
31. Sakabe S, Ozawa M, Takano R, Iwastuki-Horimoto K, Kawaoka Y. 2011. Mutations in PA, NP, andHAof a pandemic (H1N1) 2009 influenza virus contribute to its adaptation to mice. Virus Res. 158:124-129.
32. Li Z, Watanabe T, Hatta M, Watanabe S, Nanbo A, Ozawa M, Kakugawa S, Shimojima M, Yamada S, Neumann G, Kawaoka Y. 2009. Mutational analysis of conserved amino acids in the influenza A virus nucleoprotein. J. Virol. 83:4153-4162.
33. Gabriel G, Klingel K, Otte A, Thiele S, Hudjetz B, Arman-Kalcek G, Sauter M, Shmidt T, Rother F, Baumgarte S, Keiner B, Hartmann E, Bader M, Brownlee GG, Fodor E, Klenk HD. 2011. Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat. Commun. 2:156.
34. Zimmermann P, Manz B, Haller O, Schwemmle M, Kochs G. 2011. The viral nucleoprotein determines Mx sensitivity of influenza A viruses. J. Virol. 85:8133-8140.
35. Hurt AC, Nor'e SS, McCaw JM, Fryer HR, Mosse J, McLean AR, Barr IG. 2010. Assessing the viral fitness of oseltamivir-resistant influenza viruses in ferrets, using a competitive-mixtures model. J. Virol. 84:9427-9438.
36. Murcia PR, Baillie GJ, Daly J, Elton D, Jervis C, Mumford JA, Newton R, Parrish CR, Hoelzer K, Dougan G, Parkhill J, Lennard N, Ormond D, Moule S, Whitwham A, McCauley JW, McKinley TJ, Holmes EC, Grenfell BT, Wood JL. 2010. Intra- and interhost evolutionary dynamics of equine influenza virus. J. Virol. 84:6943-6954.
37. Murcia PR, Hughes J, Battista P, Lloyd L, Baillie GJ, Ramirez-Gonzalez RH, Ormond D, Oliver K, Elton D, Mumford JA, Caccamo M, Kellam P, Grenfell BT, Holmes EC, Wood JL. 2012. Evolution of an Eurasian avian-like influenza virus in naive and vaccinated pigs. PLoS Pathog. 8:e1002730. doi:10.1371/journal.ppat.1002730.
38. Seibert CW, Kaminski M, Philipp J, Rubbenstroth D, Albrecht RA, Schwalm F, Stertz S, Medina RA, Kochs G, Garcia-Sastre A, Staeheli P, Palese P. 2010. Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J. Virol. 84:11219-11226.
39. Long J, Bushnell RV, Tobin JK, Pan K, Deem MW, Nara PL, Tobin GJ. 2011. Evolution of H3N2 influenza virus in a guinea pig model. PLoS One 6:e20130. doi:10.1371/journal.pone.0020130.
40. Hoelzer K, Murcia PR, Baillie GJ, Wood JL, Metzger SM, Osterrieder N, Dubovi EJ, Holmes EC, Parrish CR. 2010. Intrahost evolutionary dynamics of canine influenza virus in naive and partially immune dogs. J. Virol. 84:5329-5335.