Protease activation mutants elicit protective immunity against highly pathogenic avian influenza viruses of subtype H7 in chickens and mice

Emerging Microbes and Infections

Volumn 2, Issue , 2013, Pages

  Wagner, Ralf ^a   Gabriel, Gülsah ^b,d   Schlesner, Matthias ^b,e   Alex, Nina ^a   Herwig, Astrid ^b   Werner, Ortrud ^c   Klenk, Hans Dieter ^b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^d LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

influenza virus; pathogenicity; protection; proteolytic activation; vaccine

Indexed keywords

AVIAN INFLUENZA VACCINE; PROTEINASE;

ANIMAL EXPERIMENT; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; ENZYME ACTIVATION; FLUOROGRAPHY; IMMUNIZATION; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; THERAPY EFFECT; VIRUS PATHOGENESIS; VIRUS REPLICATION; WILD TYPE;

AVIAN INFLUENZA VIRUS; GALLUS GALLUS; MUS; ORTHOMYXOVIRIDAE;

EID: 84878613626     PISSN: None     EISSN: 22221751     Source Type: Journal    
DOI: 10.1038/emi2013.7     Document Type: Article

References (41)

1. Alexander DJ. A review of avian influenza in different bird species. Vet Microbiol 2000; 74: 3-13. (Pubitemid 30224640)
2. Guan Y, Smith GJ, Webby R, Webster RG. Molecular epidemiology of H5N1 avian influenza. Rev Sci Tech 2009; 28: 39-47.
3. Lvov DK, Shchelkanov MY, Prilipov AG et al. Evolution of highly pathogenic avian influenza H5N1 virus in natural ecosystems of northern Eurasia (2005-08). Avian Dis 2010; 54(Suppl): 483-495.
4. Malik Peiris JS. Avian influenza viruses in humans. Rev Sci Tech 2009; 28: 161-173.
5. Kurtz J, Manvell RJ, Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 1996; 348: 901-902. (Pubitemid 26320930)
6. Taylor HR, Turner AJ. A case report of fowl plague keratoconjunctivitis. Br J Ophthalmol 1977; 61: 86-88. (Pubitemid 8162891)
7. Webster RG, Geraci J, Petursson G, Skirnisson K. Conjunctivitis in human beings caused by influenza A virus of seals. N Engl J Med 1981; 304: 911.
8. Fouchier RA, Schneeberger PM, Rozendaal FW et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA 2004; 101: 1356-1361. (Pubitemid 38182693)
9. Lipatov AS, Webby RJ, Govorkova EA, Krauss S, Webster RG. Efficacy of H5 influenza vaccines produced by reverse genetics in a lethal mouse model. J Infect Dis 2005; 191: 12160-12120.
10. Subbarao K, Chen H, Swayne D et al. Evaluation of a genetically modified reassortant H5N1 influenza A virus vaccine candidate generated by plasmid-based reverse genetics. Virology 2003; 305: 192-200. (Pubitemid 36062823)
11. Webby RJ, Perez DR, Coleman JS et al. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 2004; 363: 1099-1103. (Pubitemid 38452781)
12. Min JY, Vogel L, Matsuoka Y et al. A live attenuated H7N7 candidate vaccine virus induces neutralizing antibody that confers protection from challenge in mice, ferrets, and monkeys. J Virol 2010; 84: 11950-11960.
13. Talaat KR, Karron RA, Callahan KA et al. A live attenuated H7N3 influenza virus vaccine is well tolerated and immunogenic in a Phase I trial in healthy adults. Vaccine 2009; 27: 3744-3753.
14. Gao W, Soloff AC, Lu X et al. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 2006; 80: 1959-1964. (Pubitemid 43228735)
15. Swayne DE. Application of new vaccine technologies for the control of transboundary diseases. Dev Biol (Basel) 2004; 119: 219-228.
16. Shi H, Liu XF, Zhang X, Chen S, Sun L, Lu J. Generation of an attenuated H5N1 avian influenza virus vaccine with all eight genes from avian viruses. Vaccine 2007; 25: 7379-7384. (Pubitemid 47484015)
17. Tian G, Zhang S, Li Y et al. Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology 2005; 341: 153-162. (Pubitemid 41356582)
18. Chen H. Avian influenza vaccination: the experience in China. Rev Sci Tech 2009; 28: 267-274.
19. Klenk HD, Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol 1994; 2: 39-43. (Pubitemid 24051419)
20. Gabriel G, Garn H, WegmannMet al. The potential of a protease activation mutant of a highly pathogenic avian influenza virus for a pandemic live vaccine. Vaccine 2008; 26: 956-965.
21. Stech J, Garn H, Wegmann M, Wagner R, Klenk HD. A new approach to an influenza live vaccine: modification of the cleavage site of hemagglutinin. Nat Med 2005; 11: 683-689. (Pubitemid 40868311)
22. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 2005; 102: 18590-18595. (Pubitemid 43011270)
23. Wagner R, HerwigA, Azzouz N, Klenk HD. Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol 2005; 79: 6449-6458. (Pubitemid 40617248)
24. Neumann G, Watanabe T, Ito H et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 1999; 96: 9345-9350. (Pubitemid 29374757)
25. OIE. On avian influenza: manual of diagnostic tests and vaccines. Paris: OIE, 2009. Available at http://web.oie.int/eng/normes/mmanual/2008/pdf/2.03.04- AI.pdf (accessed 17 January 2013).
26. Stieneke-Grober A, Vey M, Angliker H et al. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 1992; 11: 2407-2414.
27. Feldmann A, Schafer MK, GartenW, Klenk HD. Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J Virol 2000; 74: 8018-8027. (Pubitemid 30641647)
28. Rott R, Reinacher M, Orlich M, Klenk HD. Cleavability of hemagglutinin determines spread of avian influenza viruses in the chorioallantoic membrane of chicken embryo. Arch Virol 1980; 65: 123-133. (Pubitemid 10012474)
29. Scheiblauer H, Kendal AP, Rott R. Pathogenicity of influenza A/Seal/Mass/1/80 virus mutants for mammalian species. Arch Virol 1995; 140: 341-348.
30. Klenk HD, Rott R, Orlich M, Blodorn J. Activation of influenza A viruses by trypsin treatment. Virology 1975; 68: 426-439.
31. Klenk HD, Garten W, Matrosovich M. Molecular mechanisms of interspecies transmission and pathogenicity of influenza viruses: lessons from the 2009 pandemic. Bioessays 2011; 33: 180-188.
32. Neumann G, Kawaoka Y. Host range restriction and pathogenicity in the context of influenza pandemic. Emerg Infect Dis 2006; 12: 881-886. (Pubitemid 43848407)
33. Steinhauer DA. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 1999; 258: 1-20. (Pubitemid 29391776)
34. Bogs J, Veits J, Gohrbandt S et al. Highly pathogenic H5N1 influenza viruses carry virulence determinants beyond the polybasic hemagglutinin cleavage site. PLoS ONE 2010; 5: e11826.
35. Stech O, Veits J, Weber S et al. Acquisition of a polybasic hemagglutinin cleavage site by a low-pathogenic avian influenza virus is not sufficient for immediate transformation into a highly pathogenic strain. J Virol 2009; 83: 5864-5868.
36. Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, Wiley DC. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 1998; 95: 409-417. (Pubitemid 28507328)
37. Robertson JS, Engelhardt OG. Developing vaccines to combat pandemic influenza. Viruses 2010; 2: 532-546.
38. World Health Organisation. WHO guidance on development of influenza vaccine reference viruses by reverse genetics. Geneva: WHO, 2012. Available at http:// www.who.int/vaccine-research/diseases/influenza/WHO-guidance-on- development-of-influenza-vaccine-reference-viruses-by-RG-2005-6.pdf (accessed 24 July 2012).
39. Glezen WP. Cell-culture-derived influenza vaccine production. Lancet 2011; 377: 698-700.
40. Minor PD, Engelhardt OG, Wood JM et al. Current challenges in implementing cellderived influenza vaccines: implications for production and regulation, July 2007, NIBSC, Potters Bar, UK. Vaccine 2009; 27: 2907-2913.
41. Minor PD. Vaccines against seasonal and pandemic influenza and the implications of changes in substrates for virus production. Clin Infect Dis 2010; 50: 560-565.