Single PA mutation as a high yield determinant of avian influenza vaccines

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Lee, Ilseob ^a   Il Kim, Jin ^a   Park, Sehee ^a   Bae, Joon Yong ^a   Yoo, Kirim ^a   Yun, Soo Hyeon ^a   Lee, Joo Yeon ^b   Kim, Kisoon ^b   Kang, Chun ^b   Park, Man Seong ^a  

^a Korea University College of Medicine   (South Korea)

^b Korea Centers for Disease Control and Prevention   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; PA PROTEIN, INFLUENZA VIRUSES; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; CHICK EMBRYO; CHLOROCEBUS AETHIOPS; ENZYME ACTIVATION; FEMALE; GENE VECTOR; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H5N1); METABOLISM; MOLECULAR MODEL; MOUSE; MUTATION; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; VACCINIA VIRUS; VERO CELL LINE; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; ANIMALS; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; ENZYME ACTIVATION; FEMALE; GENETIC ENGINEERING; GENETIC VECTORS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MICE; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; RNA REPLICASE; STRUCTURE-ACTIVITY RELATIONSHIP; VACCINIA VIRUS; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85009436168     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40675     Document Type: Article

References (68)

1. Webster, R. G. & Govorkova, E. A. Continuing challenges in influenza. Annals of the New York Academy of Sciences 1323, 115-139, doi: 10.1111/nyas.12462 (2014).
2. Herfst, S., Imai, M., Kawaoka, Y. & Fouchier, R. A. Avian influenza virus transmission to mammals. Current topics in microbiology and immunology 385, 137-155, doi: 10.1007/82-2014-387 (2014).
3. Neumann, G. & Kawaoka, Y. Transmission of influenza A viruses. Virology 479-480C, 234-246, doi: 10.1016/j.virol.2015.03.009 (2015).
4. Freidl, G. S. et al. Influenza at the animal-human interface: A review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1). Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 19 (2014).
5. WHO. (World Health Organization, 2015).
6. WHO. WHO risk assessment of Human infections with avian influenza A(H7N9) virus (reported in February 23, 2015; assessed through http://www.who.int/influenza/human-animal-interface/influenza-h7n9/RiskAssessment-H7N9-23Feb20115.pdf). (2015).
7. Herfst, S. et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534-1541, doi: 336/6088/1534 [pii]10.1126/science.1213362 (2012).
8. Imai, M. et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420-428, doi: 10.1038/nature10831 (2012).
9. Schultz-Cherry, S. & Jones, J. C. Influenza vaccines: The good, the bad, and the eggs. Advances in virus research 77, 63-84, doi: 10.1016/B978-0-12-385034-8.00003-X (2010).
10. Webby, R. J. et al. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 363, 1099-1103, doi: 10.1016/S0140-6736(04)15892-3 (2004).
11. Baz, M., Luke, C. J., Cheng, X., Jin, H. & Subbarao, K. H5N1 vaccines in humans. Virus research 178, 78-98, doi: 10.1016/j. virusres.2013.05.006 (2013).
12. Milian, E. & Kamen, A. A. Current and emerging cell culture manufacturing technologies for influenza vaccines. BioMed research international 2015, 504831, doi: 10.1155/2015/504831 (2015).
13. Lu, B., Zhou, H., Ye, D., Kemble, G. & Jin, H. Improvement of influenza A/Fujian/411/02 (H3N2) virus growth in embryonated chicken eggs by balancing the hemagglutinin and neuraminidase activities, using reverse genetics. Journal of virology 79, 6763-6771, doi: 10.1128/JVI.79.11.6763-6771.2005 (2005).
14. Robertson, J. S. et al. The development of vaccine viruses against pandemic A(H1N1) influenza. Vaccine 29, 1836-1843, doi: 10.1016/j.vaccine.2010.12.044 (2011).
15. Del Giudice, G. & Rappuoli, R. Inactivated and adjuvanted influenza vaccines. Curr Top Microbiol Immunol 386, 151-180, doi: 10.1007/82-2014-406 (2015).
16. Kang, S. M., Pushko, P., Bright, R. A., Smith, G. & Compans, R. W. Influenza virus-like particles as pandemic vaccines. Curr Top Microbiol Immunol 333, 269-289, doi: 10.1007/978-3-540-92165-3-14 (2009).
17. Perdue, M. L. et al. The future of cell culture-based influenza vaccine production. Expert review of vaccines 10, 1183-1194, doi: 10.1586/erv.11.82 (2011).
18. Lee, I., Kim, J. I. & Park, M. S. Cell culture-based influenza vaccines as alternatives to egg-based vaccines. Journal of Bacteriology and Virology 43, 9-17 (2013).
19. Govorkova, E. A., Kodihalli, S., Alymova, I. V., Fanget, B. & Webster, R. G. Growth and immunogenicity of influenza viruses cultivated in Vero or MDCK cells and in embryonated chicken eggs. Developments in biological standardization 98, 39-51; discussion 73-34 (1999).
20. Kistner, O. et al. Cell culture (Vero) derived whole virus (H5N1) vaccine based on wild-type virus strain induces cross-protective immune responses. Vaccine 25, 6028-6036, doi: 10.1016/j.vaccine.2007.05.013 (2007).
21. Vidor, E., Meschievitz, C. & Plotkin, S. Fifteen years of experience with Vero-produced enhanced potency inactivated poliovirus vaccine. The Pediatric infectious disease journal 16, 312-322 (1997).
22. Webster, R. G. & Govorkova, E. A. Continuing challenges in influenza. Annals of the New York Academy of Sciences 1323, 115-139, doi: 10.1111/nyas.12462 (2014).
23. Herfst, S., Imai, M., Kawaoka, Y. & Fouchier, R. A. Avian influenza virus transmission to mammals. Current topics in microbiology and immunology 385, 137-155, doi: 10.1007/82-2014-387 (2014).
24. Neumann, G. & Kawaoka, Y. Transmission of influenza A viruses. Virology 479-480C, 234-246, doi: 10.1016/j.virol.2015.03.009 (2015).
25. Freidl, G. S. et al. Influenza at the animal-human interface: A review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1). Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin 19 (2014).
26. WHO. (World Health Organization, 2015).
27. WHO. WHO risk assessment of Human infections with avian influenza A(H7N9) virus (reported in February 23, 2015; assessed through http://www.who.int/influenza/human-animal-interface/influenza-h7n9/RiskAssessment-H7N9-23Feb20115.pdf). (2015).
28. Herfst, S. et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534-1541, doi: 336/6088/1534 [pii]10.1126/science.1213362 (2012).
29. Imai, M. et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420-428, doi: 10.1038/nature10831 (2012).
30. Schultz-Cherry S. Jones J.C. Influenza vaccines: The good, the bad, and the eggs Advances in Virus Research 2010 77 10.1016/B978-0-12-385034-8.00003-X 63-84.
31. Webby, R. J. et al. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 363, 1099-1103, doi: 10.1016/S0140-6736(04)15892-3 (2004).
32. Baz, M., Luke, C. J., Cheng, X., Jin, H. & Subbarao, K. H5N1 vaccines in humans. Virus research 178, 78-98, doi: 10.1016/j. virusres.2013.05.006 (2013).
33. Milian, E. & Kamen, A. A. Current and emerging cell culture manufacturing technologies for influenza vaccines. BioMed research international 2015, 504831, doi: 10.1155/2015/504831 (2015).
34. Lu, B., Zhou, H., Ye, D., Kemble, G. & Jin, H. Improvement of influenza A/Fujian/411/02 (H3N2) virus growth in embryonated chicken eggs by balancing the hemagglutinin and neuraminidase activities, using reverse genetics. Journal of virology 79, 6763-6771, doi: 10.1128/JVI.79.11.6763-6771.2005 (2005).
35. Robertson, J. S. et al. The development of vaccine viruses against pandemic A(H1N1) influenza. Vaccine 29, 1836-1843, doi: 10.1016/j.vaccine.2010.12.044 (2011).
36. Del Giudice, G. & Rappuoli, R. Inactivated and adjuvanted influenza vaccines. Curr Top Microbiol Immunol 386, 151-180, doi: 10.1007/82-2014-406 (2015).
37. Kang, S. M., Pushko, P., Bright, R. A., Smith, G. & Compans, R. W. Influenza virus-like particles as pandemic vaccines. Curr Top Microbiol Immunol 333, 269-289, doi: 10.1007/978-3-540-92165-3-14 (2009).
38. Perdue, M. L. et al. The future of cell culture-based influenza vaccine production. Expert review of vaccines 10, 1183-1194, doi: 10.1586/erv.11.82 (2011).
39. Lee, I., Kim, J. I. & Park, M. S. Cell culture-based influenza vaccines as alternatives to egg-based vaccines. Journal of Bacteriology and Virology 43, 9-17 (2013).
40. Govorkova, E. A., Kodihalli, S., Alymova, I. V., Fanget, B. & Webster, R. G. Growth and immunogenicity of influenza viruses cultivated in Vero or MDCK cells and in embryonated chicken eggs. Developments in biological standardization 98, 39-51; discussion 73-34 (1999).
41. Kistner, O. et al. Cell culture (Vero) derived whole virus (H5N1) vaccine based on wild-type virus strain induces cross-protective immune responses. Vaccine 25, 6028-6036, doi: 10.1016/j.vaccine.2007.05.013 (2007).
42. Vidor, E., Meschievitz, C. & Plotkin, S. Fifteen years of experience with Vero-produced enhanced potency inactivated poliovirus vaccine. The Pediatric infectious disease journal 16, 312-322 (1997).
43. Barrett, P. N., Mundt, W., Kistner, O. & Howard, M. K. Vero cell platform in vaccine production: moving towards cell culture-based viral vaccines. Expert review of vaccines 8, 607-618, doi: 10.1586/erv.09.19 (2009).
44. Nicolson, C., Major, D., Wood, J. M. & Robertson, J. S. Generation of influenza vaccine viruses on Vero cells by reverse genetics: An H5N1 candidate vaccine strain produced under a quality system. Vaccine 23, 2943-2952, doi: 10.1016/j.vaccine.2004.08.054 (2005).
45. Murakami, S. et al. Enhanced growth of influenza vaccine seed viruses in vero cells mediated by broadening the optimal pH range for virus membrane fusion. Journal of virology 86, 1405-1410, doi: 10.1128/JVI.06009-11 (2012).
46. Tseng, Y. F. et al. Adaptation of high-growth influenza H5N1 vaccine virus in Vero cells: implications for pandemic preparedness. PloS one 6, e24057, doi: 10.1371/journal.pone.0024057 (2011).
47. Houser, K. & Subbarao, K. Influenza vaccines: challenges and solutions. Cell host & microbe 17, 295-300, doi: 10.1016/j. chom.2015.02.012 (2015).
48. Shaw, M. L. & Palese, P. In Fields Virology 1151-1185 (Lippincott Williams & Wilkins, 2013).
49. Lam, T. T. et al. Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature 522, 102-105, doi: 10.1038/nature14348 (2015).
50. Yamaji, R. et al. Mammalian Adaptive Mutations of the PA Protein of Highly Pathogenic Avian H5N1 Influenza Virus. Journal of virology 89, 4117-4125, doi: 10.1128/JVI.03532-14 (2015).
51. Dias, A. et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458, 914-918, doi: 10.1038/nature07745 (2009).
52. Xiao, S. et al. Magnesium-dependent RNA binding to the PA endonuclease domain of the avian influenza polymerase. J Phys Chem B 118, 873-889, doi: 10.1021/jp408383g (2014).
53. Arai, Y. et al. Novel Polymerase Gene Mutations for Human Adaptation in Clinical Isolates of Avian H5N1 Influenza Viruses. PLoS pathogens 12, e1005583, doi: 10.1371/journal.ppat.1005583 (2016).
54. Zhu, W., Zou, X., Zhou, J., Tang, J. & Shu, Y. Residues 41V and/or 210D in the NP protein enhance polymerase activities and potential replication of novel influenza (H7N9) viruses at low temperature. Virology journal 12, 71, doi: 10.1186/s12985-015-0304-6 (2015).
55. Hayashi, T., Wills, S., Bussey, K. A. & Takimoto, T. Identification of Influenza A Virus PB2 Residues Involved in Enhanced Polymerase Activity and Virus Growth in Mammalian Cells at Low Temperatures. Journal of virology 89, 8042-8049, doi: 10.1128/JVI.00901-15 (2015).
56. Tan, L. et al. A combination of HA and PA mutations enhances virulence in a mouse-adapted H6N6 influenza A virus. Journal of virology 88, 14116-14125, doi: 10.1128/JVI.01736-14 (2014).
57. Le, J. et al. Development of high yield reassortants for influenza type B viruses and analysis of their gene compositions. Vaccine 33, 879-884, doi: 10.1016/j.vaccine.2014.12.027 (2015).
58. Plant, E. P. & Ye, Z. Chimeric neuraminidase and mutant PB1 gene constellation improves growth and yield of H5N1 vaccine candidate virus. The Journal of general virology 96, 752-755, doi: 10.1099/jgv.0.000025 (2015).
59. Garcia-Sastre, A. et al. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252, 324-330 (1998).
60. Seitz, C., Frensing, T., Hoper, D., Kochs, G. & Reichl, U. High yields of influenza A virus in Madin-Darby canine kidney cells are promoted by an insufficient interferon-induced antiviral state. The Journal of general virology 91, 1754-1763, doi: 10.1099/vir.0.020370-0 (2010).
61. Ping, J. et al. Development of high-yield influenza A virus vaccine viruses. Nat Commun 6, 8148, doi: 10.1038/ncomms9148 (2015).
62. Kim, J. I. & Park, M. S. N-linked glycosylation in the hemagglutinin of influenza A viruses. Yonsei Med J 53, 886-893, doi: 10.3349/ymj.2012.53.5.886 (2012).
63. Kim, J. I. et al. Genetic Requirement for Hemagglutinin Glycosylation and Its Implications for Influenza A H1N1 Virus Evolution. Journal of virology 87, 7539-7549, doi: 10.1128/JVI.00373-13 (2013).
64. Tate, M. D. et al. Playing hide and seek: how glycosylation of the influenza virus hemagglutinin can modulate the immune response to infection. Viruses 6, 1294-1316, doi: 10.3390/v6031294 (2014).
65. Zhang, X. et al. Hemagglutinin glycosylation modulates the pathogenicity and antigenicity of the H5N1 avian influenza virus. Veterinary microbiology 175, 244-256, doi: 10.1016/j.vetmic.2014.12.011 (2015).
66. Fodor, E. et al. Rescue of influenza A virus from recombinant DNA. Journal of virology 73, 9679-9682 (1999).
67. Carcelli, M. et al. N-acylhydrazone inhibitors of influenza virus PA endonuclease with versatile metal binding modes. Sci Rep 6, 31500, doi: 10.1038/srep31500 (2016).
68. PyMOL. The PyMOL Molecular Graphics System, Version 1.8 Schrodinger, LLC (https://www.pymol.org/).