Genetic evolution of low pathogenecity H9N2 Avian influenza viruses in Tunisia: Acquisition of new mutations

Virology Journal

Volumn 8, Issue , 2011, Pages

  Tombari, Wafa ^a   Nsiri, Jihene ^a   Larbi, Imen ^a   Guerin, Jean ^b   Ghram, Abdeljelil ^a  

^a PASTEUR INSTITUTE OF TUNIS   (Tunisia)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; HEMAGGLUTININ; LEUCINE; MATRIX PROTEIN; NONSTRUCTURAL PROTEIN 1; NUCLEOPROTEIN; POLYMERASE PROTEIN PB2; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GLYCOSYLATION; HEMADSORPTION; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H9N2; MIDDLE EAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RECEPTOR BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TUNISIA; UNINDEXED SEQUENCE; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; AVIAN INFLUENZA; BIRD; CLASSIFICATION; DNA SEQUENCE; GENETIC REASSORTMENT; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; VIROLOGY;

AVES; AVIAN INFLUENZA VIRUS; MAMMALIA; ORTHOMYXOVIRIDAE;

ANIMALS; BIRDS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOTYPE; HUMANS; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; REASSORTANT VIRUSES; RECOMBINATION, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; TUNISIA;

EID: 80053905350     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-8-467     Document Type: Article

References (65)

1. Orthomyxoviridae: the viruses and their replication. Lamb RA, Krug RM, Fields Vrology Philadelphia Lippincott Williams & Wilkins, Knipe DM, Howley PM, Chanock RM, Melnick JL, Momath TP, Roizman S, 2001 1487 1532
2. Avian Influenza virus. Chang-Won L, Yehia MS, Comp Immun Microbiol Infec Dis 2009 32 4 301 310 10.1016/j.cimid.2008.01.007
3. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, et al. J Clin Microbiol 2005 43 5760 5767 10.1128/JCM.43.11.5760-5767. 2005 16272514 (Pubitemid 41612358)
4. Continuing evolution of H9N2 influenza viruses in Southeastern China. Choi YK, Ozaki H, Webby RJ, Webster RG, Peiris JS, Poon LL, Butt C, Leung YHC, Guan Y, J Virol 2004 78 8609 8614 10.1128/JVI.78.16.8609-8614.2004 15280470 (Pubitemid 39025127)
5. Human infection with influenza H9N2. Peiris M, Yuen KY, Leung KH, Chan PL, Lai SIp, RW M, Orr K, Shortridge KF, Lancet 1999 354 916 917 10.1016/S0140-6736(99)03311-5 10489954 (Pubitemid 29424025)
6. Cocirculation of avian H9N2 and contemporary "human" H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? Peiris S, Guan Y, Markwell D, Ghose P, Webster RG, Shortridge KF, J Virol 2001 75 9679 9686 10.1128/JVI.75.20.9679-9686.2001 11559800 (Pubitemid 32900102)
7. Discovery of humans infected by avian influenza A (H9N2) virus. Guo YJ, Li JW, Cheng I, Chin J Exp Clin Virol 1999 15 105 108
8. H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. Guan Y, Shortridge KF, Krauss S, Chin PS, Dyrting KC, Ellis TM, Webster RG, Peiris M, J virol 2000 74 9372 9380 10.1128/JVI.74.20.9372-9380.2000 11000205
9. Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. HaghighatJahromi M, Asasi K, Nili H, Dadras H, Shooshtari AH, Arch Virol 2008 153 651 655 10.1007/s00705-008-0033-x 18247102
10. Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. Kishida N, Sakoda Y, Eto M, Kida H, Arch Virol 2004 149 2095 2104 10.1007/s00705-004-0372-1 15503199 (Pubitemid 39508952)
11. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Guan Y, Shortridge KF, Krauss S, Webster RG, Proc Natl Acad Sci USA 1999 96 9363 9367 10.1073/pnas.96.16.9363 10430948 (Pubitemid 29374760)
12. Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. Wan H, Perez DR, J Virol 2007 81 5181 5191 10.1128/JVI.02827-06 17344280 (Pubitemid 46744428)
13. Manual of diagnostic tests and vaccines for terrestrial animals. OIE, Highly Pathogenic Avian Influenza OIE, Paris, France (Chapter 2.1.14), Updated on 08.07.2005
14. Update on highly pathogenic avian Influenza in animals (Type H5 and H7). OIE, http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/ 2011
15. A multiplex RT-PCR for detection of type A influenza virus and differentiation of avian H5, H7, and H9 hemagglutinin subtypes. Xie Z, Pang YS, Liu J, Deng X, Tang X, Sun J, Khan MI, Mol Cell Probes 2006 20 245 249 10.1016/j.mcp.2006.01.003 16542820
16. A simple restriction fragment length polymorphism-based strategy that can distinguish the internal genes of human H1N1, H3N2, and H5N1 influenza A viruses. Cooper LA, Subbarao K, J Clin Microbiol 2000 38 supp 7 2579 2583 10878047 (Pubitemid 30485133)
17. Recommended Laboratory Tests to Identify Avian Influenza A Virus in Specimens from Humans. WHO, 2005 http://www.who.int/csr/resources/publications/ influenza/WHO-CDS-EPR-GIP-2006-4r1.pdf
18. Molecular epizootiology of recurrent low pathogenic avian influenza by H9N2 subtype virus in Korea. Kwon HJ, Cho SH, Kim MC, Ahn YJ, Kim SJ, Avian Pathol 2006 35 4 309 315 10.1080/03079450600821166 16854644 (Pubitemid 44147746)
19. Identification and subtyping of avian influenza viruses by reverse transcription-PCR. Lee MS, Chang PC, Shien JH, Cheng MC, Shieh HK, J Virol Methods 2001 97 supp1-2 13 22 11483213 (Pubitemid 32718737)
20. Amplification of the entire genome of influenza A virus H1N1 and H3N2 subtypes by reverse-transcription polymerase chain reaction. Chi-Ho C, Keh-Liang L, You C, Ya-Li W, Yu-Tsai C, Hsiao-Li T, Happy-K S, Wu-Tse L, J Virol Method 2006 136 supp1-2 38 40
21. Characterization of a pathogenic H9N2 influenza A virus isolated from central China in 2007. Wu R, Sui ZW, Zhang HB, Chen QJ, Liang WW, Yang KL, Xiong Z, Liu ZW, Chen Z, Xu DP, Arch Virol 2008 153 1549 1555 10.1007/s00705-008- 0139-1 18574551
22. Avian influenza virus H9 subtype in poultry flocks in Jordan. Roussan DA, Khawaldeh GY, Al Rifai RH, Totanji WS, Shaheen IA, Prev Vet Med 2009 88 77 81 10.1016/j.prevetmed.2008.06.021 18692925
23. Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. Xu KM, Li KS, Smith GJ, Li JW, Tai H, Zhang JX, Webster RG, Peiris JS, Chen H, Guan Y, J Virol 2007 81 2635 2645 10.1128/JVI.02316-06 17192315 (Pubitemid 46447029)
24. Isolation and pathotyping of H9N2 avian influenza viruses in Indian poultry. Nagarajan S, Rajukumar K, Tosh C, Ramaswamy V, Purohit K, Saxena G, Behera P, Pattnaik B, Pradhan HK, Dubey SC, Vet Microbiol 2009 133 154 63 10.1016/j.vetmic.2008.06.013 18676100 (Pubitemid 50226327)
25. A Phylogenetic analysis of hemagglutinin, neuraminidase, and nucleoprotein genes of H9N2 avian influenza viruses isolated in Israel during the 2000-2005 epizootic. Perk S, Golender N, Banet-Noach C, Shihmanter E, Pokamunsky S, Pirak M, Tendler Y, Lipkind M, Panshin A, Comp Immunol Microbiol Infect Dis 2009 32 221 238 10.1016/j.cimid.2007.06.008 18249445
26. Characterization of H9 subtype influenza viruses from the ducks of southern China: a candidate for the next influenza pandemic in humans? Kwon HJ, Cho SH, Kim MC, Ahn YJLL, Yu KZ, Yuen KY, Shortridge KF, Webster RG, Guan Y, J Virol 2003 77 6988 6994 10.1128/JVI.77.12.6988-6994.2003 12768017 (Pubitemid 36666891)
27. Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. Hossain MJ, Hickman D, Perez DR, PLoS ONE 2008 3 3170 10.1371/journal.pone. 0003170 18779858
28. Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Yu H, Hua RH, Wei TC, Zhou YJ, Tian ZJ, Li GX, Liu TQ, Tong GZ, Vet Microbiol 2008 131 82 92 10.1016/j.vetmic.2008.02.024 18403137
29. Novel genotypes of H9N2 influenza A viruses isolated from poultry in Pakistan containing NS genes similar to highly pathogenic H7N3 and H5N1 viruses. Iqbal M, Yaqub T, Reddy K, McCauley JW, PLoS ONE 2009 4 5788 10.1371/journal.pone.0005788 19517011
30. A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in eastern China since 1998. Zhang P, Tang Y, Liu X, Liu W, Zhang X, Liu H, Peng D, Gao S, Wu Y, Zhang L, Lu S, J Virol 2009 83 8428 8438 10.1128/JVI.00659-09 19553328
31. Characterization of avian H9N2 influenza viruses from United Arab Emirates 2000-2003. Aamir B, Wernery U, Ilyushina N, Webster RG, Virology 2007 361 45 55 10.1016/j.virol.2006.10.037 17157891 (Pubitemid 46551216)
32. Genetic Evolution of H9 Subtype Influenza Viruses from Live Poultry Markets in Shanghai, China. Ge FF, Zhou JP, Liu J, Wang J, Zhang WY, Sheng LP, Xu F, Ju HB, Sun QY, Liu PH, J Clin Microbiol 2009 47 3294 3300 10.1128/JCM.00355-09 19656985
33. Sequence and phylogenetic analysis of the haemagglutinin genes of H9N2 avian influenza viruses isolated from commercial chickens in Iran. Homayounimehr AR, Dadras H, Shoushtari A, Pourbakhsh SA, Trop Anim Health Prod 2010 42 1291 1297 10.1007/s11250-010-9565-7 20390351
34. Virulence-associated sequence duplication at the hemagglutinin cleavage site of avian influenza viruses. Perdue ML, García M, Senne Fraire M, Virus Res 1997 49 173 186 10.1016/S0168-1702(97)01468-8 9213392 (Pubitemid 27252786)
35. Sequence requirements for cleavage activation of influenza-virus hemagglutinin expressed in mammalian-cells. Kawaoka Y, Webster RG, Proc Natl Acad Sci USA 1998 85 324 328
36. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Kawaoka Y, Webster RG, Paulson JC, Virology 1994 205 17 23 10.1006/viro.1994.1615 7975212 (Pubitemid 24360586)
37. Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I, Stevens J, Cattoli G, Capua I, Li-Mei Chen, Ruben OD, Julia B, James CP, Christy B, Richard W, Jorge B, Mohammad QAN, Daniel RP, PLoS ONE 2008 3 2923 10.1371/journal.pone.0002923 18698430
38. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Matrosovich MN, Krauss S, Webster RG, Virology 2001 281 156 162 10.1006/viro.2000.0799 11277689 (Pubitemid 32881133)
39. Mutations at the cleavage site of the hemagglutinin after the pathogenicity of influenza virus A/chick/Penn/83 (H5N2). Ohuchi M, Orlich M, Ohuchi R, Simpson BE, Garten W, Klenk HD, Rott R, Virology 1989 168 274 280 10.1016/0042-6822(89)90267-5 2916326 (Pubitemid 19073305)
40. Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. Matsuoka Y, Swayne DE, Thomas C, Rameix-Welti MA, Naffakh N, Warnes C, Altholtz M, Donis R, Subbarao K, J Virol 2009 83 470 480 10.1128/JVI.01678-08 18945774
41. Characterization of the hemagglutinin gene of subtype H9 avian influenza viruses isolated in 2007-2009 in China. Ji K, Jiang WM, Liu S, Chen JM, Chen J, Hou GY, Li JP, Huang BX, J Virol Methods 2010 163 186 189 10.1016/j.jviromet. 2009.09.013 19781574
42. Differences in receptor specificity between the influenza A viruses isolated from the duck, chicken, and human. Gambarian AS, Iamnikova SS, L'vov DK, Robertson JS, Webster RG, Matrosovich MN, Mol Biol (Mosk) 2002 36 542 549
43. Multiple amino acid substitutions are involved in the adaptation of H9N2 avian influenza virus to mice. Wu R, Zhang H, Yang K, Liang W, Xiong Z, Liu Z, Yang X, Shao H, Zheng X, Chen M, Xu D, Vet Microbiol 2009 138 85 91 10.1016/j.vetmic.2009.03.010 19342184
44. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Hatta M, Gao P, Halfmann P, Kawaoka Y, Science 2001 293 1840 1842 10.1126/science.1062882 11546875 (Pubitemid 32845783)
45. PB2 protein of a highly pathogenic avian influenza virus strain A/chicken/Yamaguchi/7/2004 (H5N1) determines its replication potential in pigs. Manzoor R, Sakoda Y, Nomura N, Tsuda Y, Ozaki H, Okamatsu M, Kida H, J Virol 2009 83 1572 1580 10.1128/JVI.01879-08 19052090
46. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627 K or 627E/701N. Steel J, Lowen AC, Mubareka S, Palese P, PLoS Pathog 2009 5 1000252 10.1371/journal.ppat.1000252 19119420
47. Mutational analysis identifies functional domains in the influenza A virus PB2 polymerase subunit. Perales B, de la Luna S, Palacios I, Ortín J, J Virol 1996 70 1678 1686 8627688 (Pubitemid 26062927)
48. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. Portela A, Digard P, J Gen Virol 2002 83 723 734 11907320 (Pubitemid 34284855)
49. Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K, J Med Virol 2002 66 107 114 10.1002/jmv.2118 11748666 (Pubitemid 34183725)
50. Genomic signatures of human versus avian influenza A viruses. Chen GW, Chang SC, Mok CK, Lo YL, Kung YN, Huang JH, Shih YH, Wang JY, Chen CJ, Shih SR, Emerg Infect Dis 2006 12 1353 1360 17073083
51. Emergence of amantadine-resistant influenza A viruses: epidemiological study. Suzuki H, Saito R, Masuda H, Oshitani H, Sato M, Sato I, J Infect Chemother 2003 9 195 200 10.1007/s10156-003-0262-6 14513385 (Pubitemid 37288281)
52. Influenza virus M2 protein has ion channel activity. Pinto LH, Holsinger LJ, Lamb RA, Cell 1992 69 517 528 10.1016/0092-8674(92)90452-I 1374685
53. A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Jackson D, Hossain MJ, Hickman D, Perez DR, Lamb RA, Proc Natl Acad Sci USA 2008 105 4381 4386 10.1073/pnas.0800482105 18334632 (Pubitemid 351754389)
54. A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, Liu W, Bu Z, Kawaokam Y, Chen H, J Virol 2008 82 1146 1154 10.1128/JVI.01698-07 18032512
55. Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3' end processing of cellular pre-mRNAS. Noah DL, Twu KY, Krug RM, Virology 2003 307 386 395 10.1016/S0042-6822(02)00127-7 12667806 (Pubitemid 36344169)
56. Mutations in the NS1 C-terminal tail do not enhance replication or virulence of the 2009 pandemic H1N1 influenza A virus. Hale BG, Steel J, Manicassamy B, Medina RA, Ye J, Hickman D, Lowen AC, Perez DR, García-Sastre A, J Gen Virol 2010 91 737 742
57. The multifunctional NS1 protein of influenza A viruses. Hale BG, Randall RE, Ortín J, Jackson D, J Gen Virol 2008 89 2359 2376 10.1099/vir.0.2008/004606-0 18796704
58. RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. Weirong W, Kelly R, Patricia L, ChenY C, Gaetano TM, Robert MK, RNA 1999 5 195 205 10.1017/S1355838299981621 10024172 (Pubitemid 29079280)
59. The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine responses. Seo SH, Hoffmann E, Webster RG, Virus Res 2004 103 107 113 10.1016/j.virusres.2004.02.022 15163498 (Pubitemid 38649069)
60. Influenza A virus NS1 gene mutations F103L and M106I increase replication and virulence. Dankar SK, Wang S, Ping J, Forbes NE, Keleta L, Li Y, Brown EG, Virol J 2011 8 13 10.1186/1743-422X-8-13 21226922
61. Glycine 184 in nonstructural protein NS1 determines the virulence of influenza A virus strain PR8 without affecting the host interferon response. Steidle S, Martínez-Sobrido L, Mordstein M, Lienenklaus S, García-Sastre A, Stäheli P, Kochs G, J Virol 2010 84 12761 1270 10.1128/JVI.00701-10 20926573
62. Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Long JX, Peng DX, Liu YL, Wu YT, Liu XF, Virus Genes 2008 36 471 480 10.1007/s11262-007-0187-8 18317917
63. Large-scale sequence analysis of avian influenza isolates. Obenauer JC, Denson JP, Mehta K, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Krauss S, Zheng J, Zhang Z, Naeve CW, Science 2006 311 1576 1580 10.1126/science.1121586 16439620
64. A specificity map for the PDZ domain family. Tonikian R, Zhang Y, Sazinsky SL, Currell BJ, Yeh H, Reva B, Held HA, Appleton BA, Evangelista M, Wu Y, Xin X, Chan AC, Seshagiri S, Lasky LA, Sander C, Boone C, Bader GD, Sidhu SS, PLoS Biol 2008 6 239 10.1371/journal.pbio.0060239 18828675
65. Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. Soubies SM, Volmer C, Croville G, Loupias J, Peralta B, Costes P, Lacroux C, Guérin JL, Volmer R, J Virol 2010 84 supp13 6733 6747 20410267