A nonpathogenic duck-origin H9N2 influenza A virus adapts to high pathogenicity in mice

Archives of Virology

Volumn 159, Issue 9, 2014, Pages 2243-2252

  Liu, Qingtao ^a   Chen, Hongzhi ^a   Huang, Junqing ^a   Chen, Yuxin ^a   Gu, Min ^a   Wang, Xiaoquan ^a   Hu, Shunlin ^a   Liu, Xiaowen ^a   Liu, Xiufan ^a  

^a YANGZHOU UNIVERSITY   (China)

Author keywords

Avian Influenza Virus; H9N2 Virus; Influenza; Influenza Virus; Mouse Lung

Indexed keywords

VIRUS PROTEIN; VIRUS RNA;

ADAPTATION; AMINO ACID SUBSTITUTION; ANIMAL; ANIMAL STRUCTURES; ARTICLE; BAGG ALBINO MOUSE; DISEASE MODEL; DNA SEQUENCE; DUCK; FEMALE; GENETICS; INFLUENZA VIRUS A H9N2; ISOLATION AND PURIFICATION; LD 50; LUNG; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; VIROLOGY; VIRULENCE; VIRUS CULTURE; VIRUS LOAD;

ADAPTATION, BIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMAL STRUCTURES; ANIMALS; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; DUCKS; FEMALE; INFLUENZA A VIRUS, H9N2 SUBTYPE; LETHAL DOSE 50; LUNG; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SERIAL PASSAGE; VIRAL LOAD; VIRAL PROTEINS; VIRULENCE;

EID: 84907874656     PISSN: 03048608     EISSN: 14328798     Source Type: Journal    
DOI: 10.1007/s00705-014-2062-y     Document Type: Article

References (57)

1. Alexander DJ (2000) A review of avian influenza in different bird species. Vet Microbiol 74:3–13
2. Ayala A, Chung CS, Lomas JL, Song GY, Doughty LA, Gregory SH, Cioffi WG, LeBlanc BW, Reichner J, Simms HH, Grutkoski PS (2002) Shock-induced neutrophil mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am J Pathol 161:2283–2294
3. Baranowski E, Ruiz-Jarabo CM, Domingo E (2001) Evolution of cell recognition by viruses. Science 292:1102–1105
4. Baudin F, Petit I, Weissenhorn W, Ruigrok RW (2001) In vitro dissection of the membrane and RNP binding activities of influenza virus M1 protein. Virology 281:102–108
5. Bi J, Deng G, Dong J, Kong F, Li X, Xu Q, Zhang M, Zhao L, Qiao J (2010) Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007–2009. PLoS One 5:e13063
6. Boivin S, Cusack S, Ruigrok RW, Hart DJ (2010) Influenza A virus polymerase: structural insights into replication and host adaptation mechanisms. J Biol Chem 285:28411–28417
7. Brown EG (1990) Increased virulence of a mouse-adapted variant of influenza A/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol 64:4523–4533
8. Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS, Guan Y (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol 43:5760–5767
9. Chen H, Bright RA, Subbarao K, Smith C, Cox NJ, Katz JM, Matsuoka Y (2007) Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res 128:159–163
10. Chin PS, Hoffmann E, Webby R, Webster RG, Guan Y, Peiris M, Shortridge KF (2002) Molecular evolution of H6 influenza viruses from poultry in Southeastern China: prevalence of H6N1 influenza viruses possessing seven A/Hong Kong/156/97 (H5N1)-like genes in poultry. J Virol 76:507–516
11. da Silva DV, Nordholm J, Madjo U, Pfeiffer A, Daniels R (2013) Assembly of subtype 1 influenza neuraminidase is driven by both the transmembrane and head domains. J Biol Chem 288:644–653
12. de Jong JC, Claas EC, Osterhaus AD, Webster RG, Lim WL (1997) A pandemic warning? Nature 389:554
13. Dong G, Luo J, Zhang H, Wang C, Duan M, Deliberto TJ, Nolte DL, Ji G, He H (2011) Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS One 6:e17212
14. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 102:18590–18595
15. Glaser L, Conenello G, Paulson J, Palese P (2007) Effective replication of human influenza viruses in mice lacking a major alpha2,6 sialyltransferase. Virus Res 126:9–18
16. Graham BS, Bunton LA, Wright PF, Karzon DT (1991) Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J Clin Invest 88:1026–1033
17. Guo Y, Li J, Cheng X (1999) Discovery of men infected by avian influenza A (H9N2) virus. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 13:105–108
18. Headley AS, Tolley E, Meduri GU (1997) Infections and the inflammatory response in acute respiratory distress syndrome. Chest 111:1306–1321
19. 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
20. Homme PJ, Easterday BC (1970) Avian influenza virus infections. I. Characteristics of influenza A-turkey-Wisconsin-1966 virus. Avian Dis 14:66–74
21. Hsieh YC, Wu TZ, Liu DP, Shao PL, Chang LY, Lu CY, Lee CY, Huang FY, Huang LM (2006) Influenza pandemics: past, present and future. J Formos Med Assoc 105:1–6
22. Jia N, Wang SX, Liu YX, Zhang PH, Zuo SQ, Lin Z, Dang RL, Ma YH, Zhang C, Zhang L, Lu S, Cao WC (2008) Increased sensitivity for detecting avian influenza-specific antibodies by a modified hemagglutination inhibition assay using horse erythrocytes. J Virol Methods 153:43–48
23. Josset L, Belser JA, Pantin-Jackwood MJ, Chang JH, Chang ST, Belisle SE, Tumpey TM, Katze MG (2012) Implication of inflammatory macrophages, nuclear receptors, and interferon regulatory factors in increased virulence of pandemic 2009 H1N1 influenza A virus after host adaptation. J Virol 86:7192–7206
24. Katz JM, Lu X, Tumpey TM, Smith CB, Shaw MW, Subbarao K (2000) Molecular correlates of influenza A H5N1 virus pathogenesis in mice. J Virol 74:10807–10810
25. Kaverin NV, Finskaya NN, Rudneva IA, Gitelman AK, Kharitonenkov IG, Smirnov YA (1989) Studies on the genetic basis of human influenza A virus adaptation to mice: degrees of virulence of reassortants with defined genetic content. Arch Virol 105:29–37
26. Kaverin NV, Rudneva IA, Ilyushina NA, Lipatov AS, Krauss S, Webster RG (2004) Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. J Virol 78:240–249
27. Kimble JB, Sorrell E, Shao H, Martin PL, Perez DR (2011) Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci USA 108:12084–12088
28. Lang JD, Figueroa M, Sanders KD, Aslan M, Liu Y, Chumley P, Freeman BA (2005) Hypercapnia via reduced rate and tidal volume contributes to lipopolysaccharide-induced lung injury. Am J Respir Crit Care Med 171:147–157
29. Lee CW, Suarez DL, Tumpey TM, Sung HW, Kwon YK, Lee YJ, Choi JG, Joh SJ, Kim MC, Lee EK, Park JM, Lu X, Katz JM, Spackman E, Swayne DE, Kim JH (2005) Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol 79:3692–3702
30. Li X, Qi W, He J, Ning Z, Hu Y, Tian J, Jiao P, Xu C, Chen J, Richt J, Ma W, Liao M (2012) Molecular basis of efficient replication and pathogenicity of H9N2 avian influenza viruses in mice. PLoS One 7:e40118
31. Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, Bu Z, Chen H (2006) The NS1 gene contributes to the virulence of H5N1 avian influenza viruses. J Virol 80:11115–11123
32. Lin YP, Shaw M, Gregory V, Cameron K, Lim W, Klimov A, Subbarao K, Guan Y, Krauss S, Shortridge K, Webster R, Cox N, Hay A (2000) Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA 97:9654–9658
33. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF (2013) Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926–1932
34. Liu Y, Lou Z, Bartlam M, Rao Z (2009) Structure-function studies of the influenza virus RNA polymerase PA subunit. Sci China C Life Sci 52:450–458
35. Majeski EI, Paintlia MK, Lopez AD, Harley RA, London SD, London L (2003) Respiratory reovirus 1/L induction of intraluminal fibrosis, a model of bronchiolitis obliterans organizing pneumonia, is dependent on T lymphocytes. Am J Pathol 163:1467–1479
36. Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281:156–162
37. Ng AK, Wang JH, Shaw PC (2009) Structure and sequence analysis of influenza A virus nucleoprotein. Sci China C Life Sci 52:439–449
38. Nick JA, Young SK, Brown KK, Avdi NJ, Arndt PG, Suratt BT, Janes MS, Henson PM, Worthen GS (2000) Role of p38 mitogen-activated protein kinase in a murine model of pulmonary inflammation. J Immunol 164:2151–2159
39. Peiris JS, Guan Y, Markwell D, Ghose P, Webster RG, Shortridge KF (2001) Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol 75:9679–9686
40. Ping J, Keleta L, Forbes NE, Dankar S, Stecho W, Tyler S, Zhou Y, Babiuk L, Weingartl H, Halpin RA, Boyne A, Bera J, Hostetler J, Fedorova NB, Proudfoot K, Katzel DA, Stockwell TB, Ghedin E, Spiro DJ, Brown EG (2011) Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS One 6:e21740
41. Reid AH, Taubenberger JK, Fanning TG (2004) Evidence of an absence: the genetic origins of the 1918 pandemic influenza virus. Nat Rev Microbiol 2:909–914
42. Rudneva IA, Kaverin NV, Varich NL, Gitelman AK, Makhov AM, Klimenko SM, Zhdanov VM (1986) Studies on the genetic determinants of influenza virus pathogenicity for mice with the use of reassortants between mouse-adapted and non-adapted variants of the same virus strain. Arch Virol 90:237–248
43. Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse-Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, Webster RG, Hoffmann E (2006) The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203:689–697
44. Scholtissek C, Rott R, Orlich M, Harms E, Rohde W (1977) Correlation of pathogenicity and gene constellation of an influenza A virus (fowl plague). I Exchange of a single gene. Virology 81:74–80
45. Shtyrya YA, Mochalova LV, Bovin NV (2009) Influenza virus neuraminidase: structure and function. Acta Nat 1:26–32
46. 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
47. Song MS, Pascua PN, Lee JH, Baek YH, Lee OJ, Kim CJ, Kim H, Webby RJ, Webster RG, Choi YK (2009) The polymerase acidic protein gene of influenza a virus contributes to pathogenicity in a mouse model. J Virol 83:12325–12335
48. Sun Y, Qin K, Wang J, Pu J, Tang Q, Hu Y, Bi Y, Zhao X, Yang H, Shu Y, Liu J (2011) High genetic compatibility and increased pathogenicity of reassortants derived from avian H9N2 and pandemic H1N1/2009 influenza viruses. Proc Natl Acad Sci USA 108:4164–4169
49. Taubenberger JK, Kash JC (2010) Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440–451
50. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, Van Rooijen N, Katz JM, Basler CF (2005) Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 79:14933–14944
51. Vines A, Wells K, Matrosovich M, Castrucci MR, Ito T, Kawaoka Y (1998) The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 72:7626–7631
52. Wan H, Perez DR (2007) Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol 81:5181–5191
53. Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I, Stevens J, Cattoli G, Capua I, Chen LM, Donis RO, Busch J, Paulson JC, Brockwell C, Webby R, Blanco J, Al-Natour MQ, Perez DR (2008) Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3:e2923
54. Xu T, Qiao J, Zhao L, He G, Li K, Wang J, Tian Y, Wang H (2009) Effect of dexamethasone on acute respiratory distress syndrome induced by the H5N1 virus in mice. Eur Respir J 33:852–860
55. Zhang P, Tang Y, Liu X, Liu W, Zhang X, Liu H, Peng D, Gao S, Wu Y, Zhang L, Lu S (2009) A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in eastern China since 1998. J Virol 83:8428–8438
56. Zhao M, Liu Q, Sun Q, Zhang W, Zhao G, Gu M, Wang X, Hu S, Liu X (2013) Full genome sequence of a natural reassortant H9N2 avian influenza virus isolated from domestic ducks in Jiangsu Province. China. Genome Announc 1:00463
57. Zhou H, Yu Z, Hu Y, Tu J, Zou W, Peng Y, Zhu J, Li Y, Zhang A, Ye Z, Chen H, Jin M (2009) The special neuraminidase stalk-motif responsible for increased virulence and pathogenesis of H5N1 influenza A virus. PLoS One 4:e6277