Genetic dynamic analysis of the influenza A H5N1 NS1 gene in China

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Wei, Kaifa ^a   Chen, Yanhui ^b   Lin, Yina ^a   Pan, Yutian ^a  

^a MINNAN NORMAL UNIVERSITY   (China)

^b TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; NONSTRUCTURAL PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RIBONUCLEOPROTEIN; VIRUS SIALIDASE; INS1 PROTEIN, INFLUENZA VIRUS; SIALIDASE; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C TERMINAL EFFECTOR DOMAIN; CHINA; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC DISTANCE; GENETIC POLYMORPHISM; GENETIC REASSORTMENT; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; INFLUENZA VIRUS A H5N1; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LUNG; MOLECULAR EVOLUTION; MOSAICISM; NONHUMAN; NS1 GENE; PHYLOGENY; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RHESUS MONKEY; SELECTIVE PRESSURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; TRANSCRIPTOMICS; UPREGULATION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS REPLICATION; ANIMAL; AVIAN INFLUENZA; BIRD; GENETIC SCREENING; GENETICS; HAPLORHINI; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS (H5N1); METABOLISM; VIROLOGY; VIRUS GENOME;

ANIMALS; BIRDS; CHINA; GENETIC TESTING; GENOME, VIRAL; HAPLORHINI; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; LUNG; NEURAMINIDASE; PHOSPHATIDYLINOSITOL 3-KINASES; PHYLOGENY; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84903899876     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101384     Document Type: Article

References (77)

1. Xu X, Subbarao, Cox NJ, Guo Y (1999) Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261: 15-19.
2. Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, et al. (1998) Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351: 467-471.
3. Chen H, Smith GJ, Li KS, Wang J, Fan XH, et al. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci U S A 103: 2845-2850.
4. Neumann G, Chen H, Gao GF, Shu Y, Kawaoka Y (2010) H5N1 influenza viruses: outbreaks and biological properties. Cell Res 20: 51-61.
5. Liu J, Xiao H, Lei F, Zhu Q, Qin K, et al. (2005) Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309: 1206.
6. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, et al. (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534-1541.
7. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, et al. (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486: 420-428.
8. Linster M, van Boheemen S, de Graaf M, Schrauwen EJ, Lexmond P, et al. (2014) Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157: 329-339.
9. Rubio L, Guerri J, Moreno P (2013) Genetic variability and evolutionary dynamics of viruses of the family Closteroviridae. Front Microbiol 4: 151.
10. Chen R, Holmes EC (2006) Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 23: 2336-2341.
11. Neverov AD, Lezhnina KV, Kondrashov AS, Bazykin GA (2014) Intrasubtype reassortments cause adaptive amino acid replacements in H3N2 influenza genes. PLoS Genet 10: e1004037.
12. Li KS, Guan Y, Wang J, Smith GJ, Xu KM, et al. (2004) Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430: 209-213.
13. Wei K, Chen Y, Xie D (2013) Genome-scale evolution and phylodynamics of H5N1 influenza virus in China during 1996-2012. Vet Microbiol 167: 383-393.
14. Chare ER, Gould EA, Holmes EC (2003) Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J Gen Virol 84: 2691-2703.
15. Simon-Loriere E, Holmes EC (2011) Why do RNA viruses recombine? Nat Rev Microbiol 9: 617-626.
16. He CQ, Xie ZX, Han GZ, Dong JB, Wang D, et al. (2009) Homologous recombination as an evolutionary force in the avian influenza A virus. Mol Biol Evol 26: 177-187.
17. 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.
18. Peiris JS, de Jong MD, Guan Y (2007) Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20: 243-267.
19. Das K, Aramini JM, Ma LC, Krug RM, Arnold E (2010) Structures of influenza A proteins and insights into antiviral drug targets. Nat Struct Mol Biol 17: 530-538.
20. Min JY, Krug RM (2006) The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 29-59 oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci U S A 103: 7100-7105.
21. Donelan NR, Basler CF, Garcia-Sastre A (2003) A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J Virol 77: 13257-13266.
22. Wei KF, Wu LJ, Chen YF, Lin YN, Wang YM, et al. (2013) Argonaute protein as a linker to command center of physiological processes. Chin J Cancer Res 25: 430-441.
23. Zhang DG, Li WZ, Wang GF, Su Y, Zeng J, et al. (2010) Heterologous SH3-p85beta inhibits influenza A virus replication. Virol J 7: 170.
24. Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y (2007) Influenza A virus NS1 protein activates the phosphatidylinositol 3-kinase (PI3K)/Akt pathway by direct interaction with the p85 subunit of PI3K. J Gen Virol 88: 13-18.
25. Hawkins PT, Anderson KE, Davidson K, Stephens LR (2006) Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 34: 647-662.
26. Ueki K, Fruman DA, Yballe CM, Fasshauer M, Klein J, et al. (2003) Positive and negative roles of p85 alpha and p85 beta regulatory subunits of phosphoinositide 3-kinase in insulin signaling. J Biol Chem 278: 48453-48466.
27. Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274.
28. Heikkinen LS, Kazlauskas A, Melen K, Wagner R, Ziegler T, et al. (2008) Avian and 1918 Spanish influenza a virus NS1 proteins bind to Crk/CrkL Src homology 3 domains to activate host cell signaling. J Biol Chem 283: 5719-5727.
29. Matsuda M, Suizu F, Hirata N, Miyazaki T, Obuse C, et al. (2010) Characterization of the interaction of influenza virus NS1 with Akt. Biochem Biophys Res Commun 395: 312-317.
30. Li Y, Anderson DH, Liu Q, Zhou Y (2008) Mechanism of influenza A virus NS1 protein interaction with the p85beta, but not the p85alpha, subunit of phosphatidylinositol 3-kinase (PI3K) and up-regulation of PI3K activity. J Biol Chem 283: 23397-23409.
31. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
32. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
33. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
34. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
35. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
36. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
37. Heath L, van der Walt E, Varsani A, Martin DP (2006) Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80: 11827-11832.
38. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, et al. (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73: 152-160.
39. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
40. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7: 256-276.
41. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
42. Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
43. Wu TT, Kabat EA (1970) An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med 132: 211-250.
44. Gribskov M, Burgess RR (1986) Sigma factors from E. coli, B. subtilis, phage SP01, and phage T4 are homologous proteins. Nucleic Acids Res 14: 6745-6763.
45. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
46. Wei KF, Chen J, Wang YM, Chen YH, Chen SX, et al. (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19: 463-476.
47. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
48. Shinya K, Gao Y, Cilloniz C, Suzuki Y, Fujie M, et al. (2012) Integrated clinical, pathologic, virologic, and transcriptomic analysis of H5N1 influenza virus-induced viral pneumonia in the rhesus macaque. J Virol 86: 6055-6066.
49. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
50. Lam TT, Chong YL, Shi M, Hon CC, Li J, et al. (2013) Systematic phylogenetic analysis of influenza A virus reveals many novel mosaic genome segments. Infect Genet Evol 18: 367-378.
51. Aguade M, Miyashita N, Langley CH (1989) Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122: 607-615.
52. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, et al. (2008) The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 4: e1000076.
53. Wei KF, Chen YF, Chen J, Wu LJ, Xie DX (2012) Evolution and adaptation of hemagglutinin gene of human H5N1 influenza virus. Virus Genes 44: 450-458.
54. Li W, Shi W, Qiao H, Ho SY, Luo A, et al. (2011) Positive selection on hemagglutinin and neuraminidase genes of H1N1 influenza viruses. Virol J 8: 183.
55. Tamuri AU, Dos Reis M, Hay AJ, Goldstein RA (2009) Identifying changes in selective constraints: host shifts in influenza. PLoS Comput Biol 5: e1000564.
56. Shi W, Gibbs MJ, Zhang Y, Zhuang D, Dun A, et al. (2008) The variable codons of H5N1 avian influenza A virus haemagglutinin genes. Sci China C Life Sci 51: 987-993.
57. Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, et al. (2006) Large-scale sequence analysis of avian influenza isolates. Science 311: 1576-1580.
58. Hale BG, Randall RE, Ortin J, Jackson D (2008) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89: 2359-2376.
59. Aragón T, de la Luna S, Novoa I, Carrasco L, Ortín J, et al. (2000) Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol Cell Biol 20: 6259-6268.
60. Carrillo B, Choi JM, Bornholdt ZA, Sankaran B, Rice AP, et al. (2014) The influenza A virus protein NS1 displays structural polymorphism. J Virol 88: 4113-4122.
61. Fan S, Macken CA, Li C, Ozawa M, Goto H, et al. (2013) Synergistic effect of the PDZ and p85beta-binding domains of the NS1 protein on virulence of an avian H5N1 influenza A virus. J Virol 87: 4861-4871.
62. Cheng A, Wong SM, Yuan YA (2009) Structural basis for dsRNA recognition by NS1 protein of influenza A virus. Cell Res 19: 187-195.
63. Das K, Ma LC, Xiao R, Radvansky B, Aramini J, et al. (2008) Structural basis for suppression of a host antiviral response by influenza A virus. Proc Natl Acad Sci U S A 105: 13093-13098.
64. Kuo RL, Krug RM (2009) Influenza a virus polymerase is an integral component of the CPSF30-NS1A protein complex in infected cells. J Virol 83: 1611-1616.
65. Wei KF, Wu LJ, Chen J, Chen YF, Xie DX (2012) Structural evolution and functional diversification analyses of argonaute protein. J Cell Biochem 113: 2576-2585.
66. Miled N, Yan Y, Hon WC, Perisic O, Zvelebil M, et al. (2007) Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit. Science 317: 239-242.
67. Li W, Wang G, Zhang H, Shen Y, Dai J, et al. (2012) Inability of NS1 protein from an H5N1 influenza virus to activate PI3K/Akt signaling pathway correlates to the enhanced virus replication upon PI3K inhibition. Vet Res 43: 36.
68. Krug RM, Yuan W, Noah DL, Latham AG (2003) Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309: 181-189.
69. Koyasu S (2003) The role of PI3K in immune cells. Nat Immunol 4: 313-319.
70. Hrincius ER, Dierkes R, Anhlan D, Wixler V, Ludwig S, et al. (2011) Phosphatidylinositol-3-kinase (PI3K) is activated by influenza virus vRNA via the pathogen pattern receptor Rig-I to promote efficient type I interferon production. Cell Microbiol 13: 1907-1919.
71. Wang J, Vijaykrishna D, Duan L, Bahl J, Zhang JX, et al. (2008) Identification of the progenitors of Indonesian and Vietnamese avian influenza A (H5N1) viruses from southern China. J Virol 82: 3405-3414.
72. Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413-429.
73. Kochs G, Garcia-Sastre A, Martínez-Sobrido L (2007) Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81: 7011-7021.
74. Munir M, Zohari S, Metreveli G, Baule C, Belák S, et al. (2011) Alleles A and B of non-structural protein 1 of avian influenza A viruses differentially inhibit beta interferon production in human and mink lung cells. J Gen Virol 92: 2111-2121.
75. Burgui I, Aragón T, Ortín J, Nieto A (2003) PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J Gen Virol 84: 3263-3274.
76. Jackson D, Hossain MJ, Hickman D, Perez DR, Lamb RA (2008) A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci U S A 105: 4381-4386.
77. Zielecki F, Semmler I, Kalthoff D, Voss D, Mauel S, et al. (2010) Virulence determinants of avian H5N1 influenza A virus in mammalian and avian hosts: role of the C-terminal ESEV motif in the viral NS1 protein. J Virol 84: 10708-10718.