Development of high-yield influenza A virus vaccine viruses

Nature Communications

Volumn 6, Issue , 2015, Pages

  Ping, Jihui ^a   Lopes, Tiago J S ^a,b   Nidom, Chairul A ^c   Ghedin, Elodie ^d,e   MacKen, Catherine A ^f   Fitch, Adam ^e   Imai, Masaki ^a   Maher, Eileen A ^a   Neumann, Gabriele ^a   Kawaoka, Yoshihiro ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c AIRLANGGA UNIVERSITY   (Indonesia)

^d NEW YORK UNIVERSITY   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; HEMAGGLUTININ; INFLUENZA VACCINE; SIALIDASE; VIRUS RNA; INFLUENZA VIRUS HEMAGGLUTININ;

BLOOD; GENE EXPRESSION; INFECTIVITY; INFLUENZA; MUTATION; PRIMATE; PROTEIN; VACCINATION; VACCINE; VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DNA LIBRARY; EMBRYO; FEMALE; GENETIC STABILITY; HEMAGGLUTINATION; HUMAN; HUMAN CELL; INFLUENZA A VIRUS (A/PUERTO RICO/8/1934(H1N1)); INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H7N9); INFLUENZA VIRUS; LD50; MDCK CELL LINE; MOUSE; NONHUMAN; PROMOTER REGION; RANDOMIZED CONTROLLED TRIAL; SITE DIRECTED MUTAGENESIS; STOP CODON; VACCINATION; VACCINE PRODUCTION; VIRUS MUTANT; WILD TYPE; ANIMAL; BIOSYNTHESIS; CHLOROCEBUS AETHIOPS; DOG; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; INFLUENZA A VIRUS; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; VERO CELL LINE;

PUERTO RICO;

CERCOPITHECUS AETHIOPS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; DOGS; HEK293 CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; MADIN DARBY CANINE KIDNEY CELLS; MOLECULAR SEQUENCE DATA; MUTATION; NEURAMINIDASE; VERO CELLS;

EID: 84940668022     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9148     Document Type: Article

References (61)

1. Wright, P. F., Neumann, G., Kawaoka, Y. in Fields Virology 6th edn (eds Knipe, D. M. et al.) (Lippincott Williams & Wilkins, 2013).
2. China-WHO Joint Mission on Human Infection with Avian Influenza A(H7N9) Virus. http://www.who.int/influenza/human-animal-interface/influenza-h7n9/ChinaH7N9JointMissionReport2013.pdf (2013).
3. Centers for Disease C, Prevention. Emergence of Avian Influenza A(H7N9) Virus Causing Severe Human Illness-China, February-April 2013. MMWR Morb Mortal Wkly Rep 62, 366-371 (2013).
4. Burnet, F. M. Influenza virus on the developing egg. I. Changes associated with the development of an egg-passage strain of virus. Br. J. Exp. Pathol. 17, 282-293 (1936).
5. Katz, J. M., Wang, M., Webster, R. G. Direct sequencing of the HA gene of influenza (H3N2) virus in original clinical samples reveals sequence identity with mammalian cell-grown virus. J. Virol. 64, 1808-1811 (1990).
6. Schild, G. C., Oxford, J. S., de Jong, J. C.,Webster, R. G. Evidence for host-cell selection of influenza virus antigenic variants. Nature 303, 706-709 (1983).
7. Gambaryan, A. S. et al. Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs. Virology 247, 170-177 (1998).
8. Katz, J. M., Naeve, C. W., Webster, R. G. Host cell-mediated variation in H3N2 influenza viruses. Virology 156, 386-395 (1987).
9. Katz, J. M., Webster, R. G. Amino acid sequence identity between the HA1 of influenza A (H3N2) viruses grown in mammalian and primary chick kidney cells. J. Gen. Virol. 73, 1159-1165 (1992).
10. Robertson, J. S. et al. Structural changes in the haemagglutinin which accompany egg adaptation of an influenza A(H1N1) virus. Virology 160, 31-37 (1987).
11. Rocha, E. P. et al. Comparison of 10 influenza A (H1N1 and H3N2) haemagglutinin sequences obtained directly from clinical specimens to those of MDCK cell-and egg-grown viruses. J. Gen. Virol. 74, 2513-2518 (1993).
12. Chen, Z., Zhou, H., Jin, H. The impact of key amino acid substitutions in the hemagglutinin of influenza A (H3N2) viruses on vaccine production and antibody response. Vaccine 28, 4079-4085 (2010).
13. Skowronski, D. M. et al. Low 2012-13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS One 9, e92153 (2014).
14. Bardiya, N., Bae, J. H. Influenza vaccines: recent advances in production technologies. Appl. Microbiol. Biotechnol. 67, 299-305 (2005).
15. Palache, A. M. et al. Safety, reactogenicity and immunogenicity of Madin Darby Canine Kidney cell-derived inactivated influenza subunit vaccine. A metaanalysis of clinical studies. Dev. Biol. Stand. 98, 115-125; discussion 133-134 (1999).
16. James, J. M. et al. Safe administration of influenza vaccine to patients with egg allergy. J. Pediatr. 133, 624-628 (1998).
17. Kistner, O. et al. Development of a mammalian cell (Vero) derived candidate influenza virus vaccine. Vaccine 16, 960-968 (1998).
18. Perdue, M. L. et al. The future of cell culture-based influenza vaccine production. Expert. Rev. Vaccines. 10, 1183-1194 (2011).
19. 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. J. Virol. 79, 6763-6771 (2005).
20. Robertson, J. S. et al. The development of vaccine viruses against pandemic A(H1N1) influenza. Vaccine 29, 1836-1843 (2011).
21. Jin, H., Chen, Z. Production of live attenuated influenza vaccines against seasonal and potential pandemic influenza viruses. Curr. Opin. Virol. 6, 34-39 (2014).
22. Harvey, R., Guilfoyle, K. A., Roseby, S., Robertson, J. S., Engelhardt, O. G. Improved antigen yield in pandemic H1N1 (2009) candidate vaccine viruses with chimeric hemagglutinin molecules. J. Virol. 85, 6086-6090 (2011).
23. Harvey, R. et al. Improved haemagglutinin antigen content in H5N1 candidate vaccine viruses with chimeric haemagglutinin molecules. Vaccine 28, 8008-8014 (2010).
24. Jing, X., Phy, K., Li, X., Ye, Z. Increased hemagglutinin content in a reassortant 2009 pandemic H1N1 influenza virus with chimeric neuraminidase containing donor A/Puerto Rico/8/34 virus transmembrane and stalk domains. Vaccine 30, 4144-4152 (2012).
25. Adamo, J. E., Liu, T., Schmeisser, F., Ye, Z. Optimizing viral protein yield of influenza virus strain A/Vietnam/1203/2004 by modification of the neuraminidase gene. J. Virol. 83, 4023-4029 (2009).
26. Gomila, R. C. et al. Improving influenza virus backbones by including terminal regions of MDCK-adapted strains on hemagglutinin and neuraminidase gene segments. Vaccine 31, 4736-4743 (2013).
27. Pan, W. et al. Improvement of influenza vaccine strain A/Vietnam/1194/2004 (H5N1) growth with the neuraminidase packaging sequence from A/Puerto Rico/8/34. Hum. Vaccin. Immunother. 8, 252-259 (2012).
28. Horimoto, T. et al. Enhanced growth of seed viruses for H5N1 influenza vaccines. Virology 366, 23-27 (2007).
29. Murakami, S. et al. Growth determinants for H5N1 influenza vaccine seed viruses in MDCK cells. J. Virol. 82, 10502-10509 (2008).
30. Shaw, M. L., Palese, P. in Fields Virology 6th edn (eds Knipe, D. M. et al.) (Lippincott Williams & Wilkins, 2013).
31. Ramanunninair, M. et al. Molecular signature of high yield (growth) influenza a virus reassortants prepared as candidate vaccine seeds. PLoS One 8, e65955 (2013).
32. Ye, Q., Krug, R. M., Tao, Y. J. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444, 1078-1082 (2006).
33. Neumann, G., Hobom, G. Mutational analysis of influenza virus promoter elements in vivo. J. Gen. Virol. 76, 1709-1717 (1995).
34. Belicha-Villanueva, A. et al. Recombinant influenza A viruses with enhanced levels of PB1 and PA viral protein expression. J. Virol. 86, 5926-5930 (2012).
35. Jiang, H. et al. Influenza virus genome C4 promoter/origin attenuates its transcription and replication activity by the low polymerase recognition activity. Virology 408, 190-196 (2010).
36. Rajakumar, A., Swierkosz, E. M., Schulze, I. T. Sequence of an influenza virus hemagglutinin determined directly from a clinical sample. Proc. Natl Acad. Sci. USA 87, 4154-4158 (1990).
37. Robertson, J. S. et al. The hemagglutinin of influenza B virus present in clinical material is a single species identical to that of mammalian cell-grown virus. Virology 179, 35-40 (1990).
38. Gambaryan, A. S. et al. Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus. Res. 114, 15-22 (2005).
39. Gambaryan, A. S., Robertson, J. S., Matrosovich, M. N. Effects of eggadaptation on the receptor-binding properties of human influenza A and B viruses. Virology 258, 232-239 (1999).
40. Gambaryan, A. S. et al. Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6'-sialyl(N-acetyllactosamine). Virology 232, 345-350 (1997).
41. Takemae, N. et al. Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs. J. Gen. Virol. 91, 938-948 (2010).
42. Stevens, J. et al. Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J. Virol. 84, 8287-8299 (2010).
43. Gatherer, D. Passage in egg culture is a major cause of apparent positive selection in influenza B hemagglutinin. J. Med. Virol. 82, 123-127 (2010).
44. Lugovtsev, V. Y., Smith, D. F., Weir, J. P. Changes of the receptor-binding properties of influenza B virus B/Victoria/504/2000 during adaptation in chicken eggs. Virology 394, 218-226 (2009).
45. Lugovtsev, V. Y., Vodeiko, G. M., Levandowski, R. A. Mutational pattern of influenza B viruses adapted to high growth replication in embryonated eggs. Virus. Res. 109, 149-157 (2005).
46. Dumitrescu, M. R., Grobnicu, M., Zilisteanu, E., Alexandrescu, V. A three years experience in using MDCK cell line for influenza virus isolation (1979-1981). Arch. Roum. Pathol. Exp. Microbiol. 40, 313-316 (1981).
47. Monto, A. S., Maassab, H. F., Bryan, E. R. Relative efficacy of embryonated eggs and cell culture for isolation of contemporary influenza viruses. J. Clin. Microbiol. 13, 233-235 (1981).
48. Alymova et al. Immunogenicity and protective efficacy in mice of influenza B virus vaccines grown in mammalian cells or embryonated chicken eggs. J. Virol. 72, 4472-4477 (1998).
49. Katz, J. M., Webster, R. G. Efficacy of inactivated influenza A virus (H3N2) vaccines grown in mammalian cells or embryonated eggs. J. Infect. Dis. 160, 191-198 (1989).
50. Newman, R. W. et al. Immune response of human volunteers and animals to vaccination with egg-grown influenza A (H1N1) virus is influenced by three amino acid substitutions in the haemagglutinin molecule. Vaccine 11, 400-406 (1993).
51. Wood, J. M. et al. Influenza A (H1N1) vaccine efficacy in animal models is influenced by two amino acid substitutions in the hemagglutinin molecule. Virology 171, 214-221 (1989).
52. Minor, P. D. Vaccines against seasonal and pandemic influenza and the implications of changes in substrates for virus production. Clin. Infect. Dis. 50, 560-565 (2010).
53. Montagnon, B. J., Fanget, B., Nicolas, A. J. The large-scale cultivation of VERO cells in micro-carrier culture for virus vaccine production. Preliminary results for killed poliovirus vaccine. Dev. Biol. Stand. 47, 55-64 (1981).
54. Dureux, B. et al. Rabies vaccine for human use, cultivated on Vero cells. Lancet 2, 98 (1986).
55. Monath, T. P. et al. ACAM2000 clonal Vero cell culture vaccinia virus (New York City Board of Health strain)-a second-generation smallpox vaccine for biological defense. Int. J. Infect. Dis. 8 Suppl 2, S31-S44 (2004).
56. Rolling, T. et al. Adaptive mutations resulting in enhanced polymerase activity contribute to high virulence of influenza A virus in mice. J. Virol. 83, 6673-6680 (2009).
57. Pflug, A., Guilligay, D., Reich, S., Cusack, S. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516, 355-360 (2014).
58. Plant, E. P., Liu, T. M., Xie, H., Ye, Z. Mutations to A/Puerto Rico/8/34 PB1 gene improves seasonal reassortant influenza A virus growth kinetics. Vaccine 31, 207-212 (2012).
59. 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 (2012).
60. Neumann, G. et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl Acad. Sci. USA 96, 9345-9350 (1999).
61. Zhou, B. et al. Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J. Virol. 83, 10309-10313 (2009).