A single E627K mutation in the PB2 protein of H9N2 Avian influenza virus increases virulence by inducing higher glucocorticoids (GCs) level

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Tian, Jin ^a,b   Qi, Wenbao ^a,b   Li, Xiaokang ^c   He, Jun ^a,b   Jiao, Peirong ^a,b   Zhang, Changhui ^a,b   Liu, Guo Qian ^a,b   Liao, Ming ^a,b  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b MOA Key Laboratory for Animal Vaccine Development   (China)

^c HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GLUCOCORTICOID; PB2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; CELL MATURATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; GENE MUTATION; INFLAMMATORY CELL; INFLUENZA VIRUS A H9N2; LYMPHOCYTE COUNT; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; T LYMPHOCYTE; THYMOCYTE; VIRUS VIRULENCE;

AMINO ACID SUBSTITUTION; ANIMALS; CHEMOKINES; CYTOKINES; GLUCOCORTICOIDS; INFLUENZA A VIRUS, H9N2 SUBTYPE; MICE; MUTATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA REPLICASE; VIRAL PROTEINS; VIRULENCE;

EID: 84862226996     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038233     Document Type: Article

References (46)

1. Hossain MJ, Hickman D, Perez DR, et al. (2008) Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One 3: e3170.
2. Deng G, Bi J, Kong F, Li X, Xu Q, (2010) Acute respiratory distress syndrome induced by H9N2 virus in mice. Arch Virol 155: 187-95.
3. Park KJ, Kwon HI, Song MS, Pascua PN, Baek YH, et al. (2011) Rapid evolution of low-pathogenic H9N2 avian influenza viruses following poultry vaccination programmes. J Gen Virol 92: 36-50.
4. Guan Y, Shortridge KF, Krauss S, Chin PS, Dyrting KC, et al. (2000) H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. J Virol 74: 9372-80.
5. Pinghu Zhang YT, Xiaowen Liu, Wenbo Liu, Xiaorong Zhang, Hongqi Liu, et al. (2009) A Novel Genotype H9N2 Infl{ligature}uenza Virus Possessing Human H5N1 Internal Genomes Has Been Circulating in Poultry in Eastern China since 1998. JOURNAL OF VIROLOGY 83: 8428-38.
6. Lee DC, Mok CK, Law AH, Peiris M, Lau AS, (2010) Differential replication of avian influenza H9N2 viruses in human alveolar epithelial A549 cells. Virol J 7: 71.
7. Sorrell EM, Wan H, Araya Y, Song H, Perez DR, (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A 106: 7565-70.
8. Kim HR, Park CK, Oem JK, Bae YC, Choi JG, et al. (2010) Characterization of H5N2 influenza viruses isolated in South Korea and their influence on the emergence of a novel H9N2 influenza virus. J Gen Virol 91: 1978-83.
9. Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, et al. (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol 43: 5760-7.
10. Lin YP, Shaw M, Gregory V, Cameron K, Lim W, et al. (2000) Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci U S A 97: 9654-8.
11. Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, et al. (2008) Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3: e2923.
12. Wu R, Liu Z, Liang W, Yang K, Xiong Z, et al. (2010) Transmission of avian H9N2 infl{ligature}uenza viruses in a murine model. Veterinary Microbiology 142: 211-6.
13. Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, et al. (2000) Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 267: 279-88.
14. Bi J, Deng G, Dong J, Kong F, Li X, et al. (2010) Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007-2009. PLoS One 5.
15. Li J, Prudence M, Xi X, Hu T, Liu Q, et al. (2009) Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian infl{ligature}uenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. Virus Research 144: 123-9.
16. Aggarwal S, Dewhurst S, Takimoto T, Kim B, (2011) Biochemical Impact of the Host Adaptation-associated PB2 E627K Mutation on the Temperature-dependent RNA Synthesis Kinetics of Influenza A Virus Polymerase Complex. J Biol Chem 286: 34504-13.
17. Fornek JL, Gillim-Ross L, Santos C, Carter V, Ward JM, et al. (2009) A single-amino-acid substitution in a polymerase protein of an H5N1 influenza virus is associated with systemic infection and impaired T-cell activation in mice. J Virol 83: 11102-15.
18. Wu R, Zhang H, Yang K, Liang W, Xiong Z, et al. (2009) Multiple amino acid substitutions are involved in the adaptation of H9N2 avian influenza virus to mice. Vet Microbiol 138: 85-91.
19. Tumpey TM, Lu X, Morken T, Zaki SR, Katz JM, (2000) Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J Virol 74: 6105-16.
20. Bhattacharyya S, Zhao Y, Kay TW, Muglia LJ, (2011) Glucocorticoids target suppressor of cytokine signaling 1 (SOCS1) and type 1 interferons to regulate Toll-like receptor-induced STAT1 activation. Proc Natl Acad Sci U S A 108: 9554-9.
21. Jamieson AM, Yu S, Annicelli CH, Medzhitov R, (2010) Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe 7: 103-14.
22. Aldridge JR, Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, et al. (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106: 5306-11.
23. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C, (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 184: 39-51.
24. Xie D, Bai H, Liu L, Xie X, Ayello J, et al. (2009) Apoptosis of lymphocytes and monocytes infected with influenza virus might be the mechanism of combating virus and causing secondary infection by influenza. Int Immunol 21: 1251-62.
25. Tarendeau F, Crepin T, Guilligay D, Ruigrok RW, Cusack S, et al. (2008) Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4: e1000136.
26. Subbarao EK, London W, Murphy BR, (1993) A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67: 1761-4.
27. Julkunen I, Melén K, Nyqvist M, Pirhonen J, Sareneva T, et al. (2001) Infl{ligature}ammatory responses in infl{ligature}uenza A virus infection. Vaccine 19: 6.
28. Peiris JSK, Cheung CY, Leung CYH, Nicholls JM, (2009) Innate immune responses to infl{ligature}uenza A H5N1:friendorfoe? Cell.Rev 747: 11.
29. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, et al. (2009) Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A 106: 3455-60.
30. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM, (2008) H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4: e1000115.
31. Berg RE, Forman J, (2006) The role of CD8 T cells in innate immunity and in antigen non-specific protection. Curr Opin Immunol 18: 338-43.
32. Brincks EL, Katewa A, Kucaba TA, Griffith TS, Legge KL, (2008) CD8 T cells utilize TRAIL to control influenza virus infection. J Immunol 181: 4918-25.
33. Teijaro JR, Walsh KB, Cahalan S, Fremgen DM, Roberts E, et al. (2011) Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146: 980-91.
34. Bot A, Bot S, Bona CA, (1998) Protective role of gamma interferon during the recall response to influenza virus. J Virol 72: 6637-45.
35. Vogel AB, Haasbach E, Reiling SJ, Droebner K, Klingel K, et al. (2010) Highly pathogenic influenza virus infection of the thymus interferes with T lymphocyte development. J Immunol 185: 4824-34.
36. Teodoro JG, Branton PE, (1997) Regulation of apoptosis by viral gene products. J Virol 71: 1739-46.
37. Takizawa T, Nakanishi Y, (2010) Role and Pathological Significance of Apoptosis Induced by Influenza Virus Infection. The Open Antimicrobial Agents Journal 2: 22-5.
38. Brewer JA, Kanagawa O, Sleckman BP, Muglia LJ, (2002) Thymocyte apoptosis induced by T cell activation is mediated by glucocorticoids in vivo. J Immunol 169: 1837-43.
39. Hughes FM Jr, Cidlowski JA, (1998) Glucocorticoid-induced thymocyte apoptosis: protease-dependent activation of cell shrinkage and DNA degradation. J Steroid Biochem Mol Biol 65: 207-17.
40. Wilckens T, De Rijk R, (1997) Glucocorticoids and immune function: unknown dimensions and new frontiers. Immunol Today 18: 418-24.
41. Wiegers GJ, Knoflach M, Bock G, Niederegger H, Dietrich H, et al. (2001) CD4(+)CD8(+)TCR(low) thymocytes express low levels of glucocorticoid receptors while being sensitive to glucocorticoid-induced apoptosis. Eur J Immunol 31: 2293-301.
42. Elftman MD, Hunzeker JT, Mellinger JC, Bonneau RH, Norbury CC, et al. (2010) Stress-induced glucocorticoids at the earliest stages of herpes simplex virus-1 infection suppress subsequent antiviral immunity, implicating impaired dendritic cell function. J Immunol 184: 1867-75.
43. Han K, Ma H, An X, Su Y, Chen J, et al. (2011) Early use of glucocorticoids was a risk factor for critical disease and death from pH1N1 infection. Clin Infect Dis 53: 326-33.
44. Herold MJ, McPherson KG, Reichardt HM, (2006) Glucocorticoids in T cell apoptosis and function. Cell Mol Life Sci 63: 60-72.
45. Silverman MN, Pearce BD, Biron CA, Miller AH, (2005) Immune modulation of the hypothalamic-pituitary-adrenal (HPA) axis during viral infection. Viral Immunol 18: 41-78.
46. Chrousos GP, (2000) The stress response and immune function: clinical implications. The 1999 Novera H. Spector Lecture. Ann N Y Acad Sci 917: 38-67.