PB2-588 v promotes the mammalian adaptation of H10N8, H7N9 and H9N2 avian influenza viruses

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Xiao, Chencheng ^a   Ma, Wenjun ^b   Sun, Na ^a   Huang, Lihong ^a   Li, Yaling ^a   Zeng, Zhaoyong ^a   Wen, Yijun ^a   Zhang, Zaoyue ^a   Li, Huanan ^a   Li, Qian ^a   Yu, Yuandi ^a   Zheng, Yi ^a   Liu, Shukai ^a   Hu, Pingsheng ^a   Zhang, Xu ^a   Ning, Zhangyong ^a   Qi, Wenbao ^a   Liao, Ming ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; HUMAN VERSUS ANIMAL COMPARISON; INFLUENZA A VIRUS (H10N8); INFLUENZA A VIRUS (H7N9); INFLUENZA A VIRUS (H9N2); MAMMAL; NONHUMAN; VIRULENCE; ADAPTATION; AMINO ACID SUBSTITUTION; ANIMAL; AVIAN INFLUENZA; BAGG ALBINO MOUSE; BIRD; CHICKEN; CHINA; DOG; FEMALE; GENETICS; HEK293 CELL LINE; HUMAN; INFLUENZA; MDCK CELL LINE; MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMALS; BIRDS; CHICKENS; CHINA; DOGS; FEMALE; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS, H10N8 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MAMMALS; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; RNA REPLICASE; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 84955322615     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19474     Document Type: Article

References (63)

1. Medina, R. A. & Garciá-Sastre, A. Influenza A viruses: new research developments. Nature Reviews Microbiology 9, 590-603 (2011).
2. Hoffmann, E., Lipatov, A. S., Webby, R. J., Govorkova, E. A. & Webster, R. G. Role of specific hemagglutinin amino acids in the immunogenicity and protection of H5N1 influenza virus vaccines. Proc Natl Acad Sci USA 102, 12915-12920 (2005).
3. Yoon, S. W., Webby, R. J. & Webster, R. G. Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol 385, 359-375 (2014).
4. Neumann, G., Noda, T. & Kawaoka, Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939 (2009).
5. Claas, E. C. et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351, 472-477 (1998).
6. Subbarao, K. et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393-396 (1998).
7. Yuen, K. Y. et al. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351, 467-471 (1998).
8. Puzelli, S. et al. Human infection with highly pathogenic A(H7N7) avian influenza virus, Italy, 2013. Emerg Infect Dis 20, 1745-1749 (2014).
9. Peiris, M. et al. Human infection with influenza H9N2. Lancet 354, 916-917 (1999).
10. Chen, Y. et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381, 1916-1925 (2013).
11. Chen, H. et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383, 714-721 (2014).
12. Qi, W. et al. Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry, China. Euro Surveill. http://dx.doi.org/10.2807/1560-7917.ES2014.19.25.20841 (2014).
13. Van Ranst, M. & Lemey, P. Genesis of avian-origin H7N9 influenza A viruses. Lancet 381, 1883-1885 (2013).
14. Ma, C. et al. Emergence and evolution of H10 subtype influenza viruses in poultry in China. J Virol 89, 3534-3541 (2015).
15. Kucharski, A. J., Mills, H. L., Donnelly, C. A. & Riley, S. Transmission Potential of Influenza A(H7N9) Virus, China, 2013-2014. Emerg Infect Dis 21, 852-855 (2015).
16. Liu, M. et al. Genetic Diversity of Avian Influenza A (H10N8) Virus in Live Poultry Markets and Its Association with Human Infections in China. Sci Rep 5, 7632 (2015).
17. Shi, Y. et al. Structures and receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses. Science 342, 243-247 (2013).
18. Xiong, X. et al. Receptor binding by an H7N9 influenza virus from humans. Nature 499, 496-499 (2013).
19. Wang, M. et al. Structural basis for preferential avian receptor binding by the human-infecting H10N8 avian influenza virus. Nat Commun 6, 5600 (2015).
20. Zhang, H. et al. A Human-Infecting H10N8 Influenza Virus Retains a Strong Preference for Avian-type Receptors. Cell Host Microbe 17, 377-384 (2015).
21. Manz, B., Schwemmle, M. & Brunotte, L. Adaptation of Avian Influenza A Virus Polymerase in Mammals To Overcome the Host Species Barrier. J Virol 87, 7200-7209 (2013).
22. Subbarao, E. K., London, W. & Murphy, B. R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67, 1761-1764 (1993).
23. De Wit, E. et al. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol 84, 1597-1606 (2010).
24. Tian, J. et al. A single E627K mutation in the PB2 protein of H9N2 avian influenza virus increases virulence by inducing higher glucocorticoids (GCs) level. PLoS One 7, e38233 (2012).
25. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840-1842 (2001).
26. Li, Z. et al. Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79, 12058-12064 (2005).
27. Gabriel, G. et al. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 102, 18590-18595 (2005).
28. Gabriel, G., Herwig, A. & Klenk, H. D. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog 4, e11 (2008).
29. Czudai-Matwich, V., Otte, A., Matrosovich, M., Gabriel, G. & Klenk, H. D. PB2 Mutations D701N and S714R Promote Adaptation of an Influenza H5N1 Virus to a Mammalian Host. J Virol 88, 8735-8742 (2014).
30. Song, W. et al. The K526R substitution in viral protein PB2 enhances the effects of E627K on influenza virus replication. Nature Communications 5, 5509 (2014).
31. Fan, S. et al. Novel residues in avian influenza virus PB2 protein affect virulence in mammalian hosts. Nat Commun 5, 5021 (2014).
32. Bi, Y. et al. Assessment of the internal genes of influenza A (H7N9) virus contributing to high pathogenicity in mice. J Virol 89, 2-13 (2015).
33. Zhang, H. et al. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. J Gen Virol 95, 779-786 (2014).
34. Yamayoshi, S. et al. Amino acids substitutions in the PB2 protein of H7N9 influenza A viruses are important for virulence in mammalian hosts. Sci Rep 5, 8039 (2015).
35. Mok, C. K. et al. Amino acid substitutions in polymerase basic protein 2 gene contribute to the pathogenicity of the novel A/H7N9 influenza virus in mammalian hosts. J Virol 88, 3568-3576 (2014).
36. Li, X. et al. Molecular basis of efficient replication and pathogenicity of H9N2 avian influenza viruses in mice. PLoS One 7, e40118 (2012).
37. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. Vol. 293 1840-18422001).
38. Bussey, K. A., Bousse, T. L., Desmet, E. A., Kim, B. & Takimoto, T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol 84, 4395-4406 (2010).
39. Huang, Y. et al. Human infection with an avian influenza A (H9N2) virus in the middle region of China. J Med Virol 87, 1641-1648 (2015).
40. Kalthoff, D. et al. Avian influenza H7N9/13 and H7N7/13: a comparative virulence study in chickens, pigeons, and ferrets. J Virol 88, 9153-9165 (2014).
41. Deng, G. et al. Genetics, receptor binding, and virulence in mice of H10N8 influenza viruses isolated from ducks and chickens in live poultry markets in China. J Virol 69, 6506-6510 (2015).
42. Vachieri, S. G. et al. Receptor binding by H10 influenza viruses. Nature 511, 475-477(2014).
43. Xu, Y. et al. Identification of the source of A (H10N8) virus causing human infection. Infect Genet Evol 30C, 159-163 (2014).
44. Lam, T. T. et al. Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature 522, 102-105 (2015).
45. Cui, L. et al. Dynamic reassortments and genetic heterogeneity of the human-infecting influenza A (H7N9) virus. Nat Commun 5, 3142 (2014).
46. Steel, J., Lowen, A. C., Mubareka, S. & Palese, P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5, e1000252 (2009).
47. Neumann, G., Macken, C. A. & Kawaoka, Y. Identification of amino acid changes that may have been critical for the genesis of A(H7N9) influenza viruses. J Virol 88, 4877-4896 (2014).
48. Miotto, O., Heiny, A., Tan, T. W., August, J. T. & Brusic, V. Identification of human-to-human transmissibility factors in PB2 proteins of influenza A by large-scale mutual information analysis. BMC Bioinformatics 9 Suppl 1, S18 (2008).
49. Yamayoshi, S. et al. Virulence-affecting amino acid changes in the PA protein of H7N9 influenza A viruses. J Virol 88, 3127-3134 (2014).
50. Shinya, K. et al. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320, 258-266 (2004).
51. Yamada, S. et al. Biological and structural characterization of a host-adapting amino acid in influenza virus. PLoS Pathog 6, e1001034 (2010).
52. Tarendeau, F. et al. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4, e1000136 (2008).
53. Reich, S. et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature 516, 361-366 (2014).
54. Pflug, A., Guilligay, D., Reich, S. & Cusack, S. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516, 355-360 (2014).
55. Mehle, A. & Doudna, J. A. Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci USA 106, 21312-21316 (2009).
56. Zhao, Z. et al. PB2-588I enhances 2009 H1N1 pandemic influenza virus virulence by increasing viral replication and exacerbating PB2 inhibition of beta interferon expression. J Virol 88, 2260-2267 (2014).
57. Watanabe, T., Watanabe, S. & Kawaoka, Y. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 7, 427-439 (2010).
58. Gabriel, G. et al. Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat Commun 2, 156 (2011).
59. Hudjetz, B. & Gabriel, G. Human-like PB2 627K Influenza Virus Polymerase Activity Is Regulated by Importin-alpha1 and-alpha7. PLoS Pathog 8, e1002488 (2012).
60. Weber, M. et al. Influenza Virus Adaptation PB2-627K Modulates Nucleocapsid Inhibition by the Pathogen Sensor RIG-I. Cell Host Microbe 17, 309-319 (2015).
61. Zhang, Q. et al. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341, 410-414 (2013).
62. Long, J. S. et al. The effect of the PB2 mutation 627K on highly pathogenic H5N1 avian influenza virus is dependent on the virus lineage. J Virol 87, 9983-9996 (2013).
63. Massin, P., Rodrigues, P., Marasescu, M., Van der Werf, S. & Naffakh, N. Cloning of the chicken RNA polymerase I promoter and use for reverse genetics of influenza A viruses in avian cells. J Virol 79, 13811-13816 (2005).