Development of broadly reactive H5N1 vaccine against different Egyptian H5N1 viruses

Vaccine

Volumn 33, Issue 23, 2015, Pages 2670-2677

  Ibrahim, Mahmoud ^a,b   Sultan, Hesham A ^b   Razik, Alaa G Abdel ^b   Kang, Kyung Il ^a   Arafa, Abdel Satar ^d   Shehata, Awad A ^b   Saif, Yehia M ^a,c   Lee, Chang Won ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b University of Sadat City   (Egypt)

^c OHIO STATE UNIVERSITY   (United States)

^d Agriculture Research Center   (Egypt)

Author keywords

Antigenicity; H5N1; HPAI; In vitro mutagenesis; Reverse genetics

Indexed keywords

AMINO ACID; AVIAN INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; HEMAGGLUTININ, AVIAN INFLUENZA A VIRUS; INFLUENZA VACCINE; MUTANT PROTEIN;

AMINO ACID SUBSTITUTION; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DRUG EFFICACY; EGYPT; EGYPTIAN; GENETIC VARIABILITY; GLYCOSYLATION; HEMAGGLUTINATION INHIBITION TEST; IMMUNOREACTIVITY; IN VITRO STUDY; INFLUENZA VIRUS A H5N1; MUTAGENESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; REVERSE GENETICS; VIRUS ISOLATION; VIRUS MUTANT; WILD TYPE; ANIMAL; CHICKEN; CROSS PROTECTION; GENETICS; GENOTYPE; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H5N1); INFLUENZA IN BIRDS; ISOLATION AND PURIFICATION; SERODIAGNOSIS; VIROLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; CHICKENS; CROSS PROTECTION; CROSS REACTIONS; EGYPT; GENOTYPE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA VACCINES; MUTAGENESIS; MUTANT PROTEINS; NEUTRALIZATION TESTS; REVERSE GENETICS;

EID: 84929047185     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.04.023     Document Type: Article

References (58)

1. Xu X., Subbarao, Cox N.J., Guo Y. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 1999, 261:15-19.
2. Aly M.M., Arafa A., Hassan M.K. Epidemiological findings of outbreaks of disease caused by highly pathogenic H5N1 avian influenza virus in poultry in Egypt during 2006. Avian Dis 2008, 52:269-277.
3. Meleigy M. Egypt battles with avian influenza. Lancet 2007, 370:553-554.
4. Peyre M., Samaha H., Makonnen Y.J., Saad A., Abd-Elnabi A., Galal S., et al. Avian influenza vaccination in Egypt: limitations of the current strategy. J Mol Genet Med 2009, 3:198-204.
5. Abdelwhab e.-S., Arafa A.S., Erfan A.M., Aly M.M., Hafez H.M. Modified H5 real-time reverse transcriptase-PCR oligonucleotides for detection of divergent avian influenza H5N1 viruses in Egypt. Avian Dis 2010, 54:1301-1305.
6. Arafa A., Suarez D.L., Hassan M.K., Aly M.M. Phylogenetic analysis of hemagglutinin and neuraminidase genes of highly pathogenic avian influenza H5N1 Egyptian strains isolated from 2006 to 2008 indicates heterogeneity with multiple distinct sublineages. Avian Dis 2010, 54:345-349.
7. Balish A.L., Davis C.T., Saad M.D., El-Sayed N., Esmat H., Tjaden J.A., et al. Antigenic and genetic diversity of highly pathogenic avian influenza A (H5N1) viruses isolated in Egypt. Avian Dis 2010, 54:329-334.
8. Cattoli G., Monne I., Fusaro A., Joannis T.M., Lombin L.H., Aly M.M., et al. Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS ONE 2009, 4:e4842.
9. WHO/OIE/FAO H5N1 Evolution Working Group (2009): continuing progress towards a unified nomenclature for the highly pathogenic H5N1 avian influenza viruses: divergence of clade 2.2 viruses. Influenza Other Respir Viruses 2009, 3:59-62.
10. WHO/OIE/FAO H5N1 Evolution Working Group. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respir Viruses 2012, 6:1-5.
11. Beato M.S., Mancin M., Yang J., Buratin A., Ruffa M., Maniero S., et al. Antigenic characterization of recent H5N1 highly pathogenic avian influenza viruses circulating in Egyptian poultry. Virology 2012, 435:350-356.
12. Ibrahim M., Eladl A.F., Sultan H.A., Arafa A.S., Abdel Razik A.G., Abd El Rahman S., et al. Antigenic analysis of H5N1 highly pathogenic avian influenza viruses circulating in Egypt (2006-2012). Vet Microbiol 2013, 167:651-661.
13. Watanabe Y., Ibrahim M.S., Ellakany H.F., Kawashita N., Daidoji T., Takagi T., et al. Antigenic analysis of highly pathogenic avian influenza virus H5N1 sublineages co-circulating in Egypt. J Gen Virol 2012, 93:2215-2226.
14. Abdelwhab E.M., Grund C., Aly M.M., Beer M., Harder T.C., Hafez H.M. Multiple dose vaccination with heterologous H5N2 vaccine: immune response and protection against variant clade 2.2.1 highly pathogenic avian influenza H5N1 in broiler breeder chickens. Vaccine 2011, 29:6219-6225.
15. Abdelwhab E.M., Grund C., Aly M.M., Beer M., Harder T.C., Hafez H.M. Influence of maternal immunity on vaccine efficacy and susceptibility of one day old chicks against Egyptian highly pathogenic avian influenza H5N1. Vet Microbiol 2012, 155:13-20.
16. Grund C., Abdelwhab e.-S., Arafa A.S., Ziller M., Hassan M.K., Aly M.M., et al. Highly pathogenic avian influenza virus H5N1 from Egypt escapes vaccine-induced immunity but confers clinical protection against a heterologous clade 2.2.1 Egyptian isolate. Vaccine 2011, 29:5567-5573.
17. Kilany W.H., Abdelwhab E.M., Arafa A.S., Selim A., Safwat M., Nawar A.A., et al. Protective efficacy of H5 inactivated vaccines in meat turkey poults after challenge with Egyptian variant highly pathogenic avian influenza H5N1 virus. Vet Microbiol 2011, 150:28-34.
18. El-Zoghby E.F., Arafa A.S., Kilany W.H., Aly M.M., Abdelwhab E.M., Hafez H.M. Isolation of avian influenza H5N1 virus from vaccinated commercial layer flock in Egypt. Virol J 2012, 9:294.
19. Hafez M.H., Arafa A., Abdelwhab E.M., Selim A., Khoulosy S.G., Hassan M.K., et al. Avian influenza H5N1 virus infections in vaccinated commercial and backyard poultry in Egypt. Poult Sci 2010, 89:1609-1613.
20. Fan J., Liang X., Horton M.S., Perry H.C., Citron M.P., Heidecker G.J., et al. Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 2004, 22:2993-3003.
21. Pica N., Hai R., Krammer F., Wang T.T., Maamary J., Eggink D., et al. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc Natl Acad Sci USA 2012, 109:2573-2578.
22. Wang T.T., Tan G.S., Hai R., Pica N., Ngai L., Ekiert D.C., et al. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc Natl Acad Sci USA 2010, 107:18979-18984.
23. Gocnik M., Fislova T., Mucha V., Sladkova T., Russ G., Kostolansky F., et al. Antibodies induced by the HA2 glycopolypeptide of influenza virus haemagglutinin improve recovery from influenza A virus infection. J Gen Virol 2008, 89:958-967.
24. Jegerlehner A., Schmitz N., Storni T., Bachmann M.F. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J Immunol 2004, 172:5598-5605.
25. Forrest H.L., Khalenkov A.M., Govorkova E.A., Kim J.K., Del Giudice G., Webster R.G. Single- and multiple-clade influenza A H5N1 vaccines induce cross protection in ferrets. Vaccine 2009, 27:4187-4195.
26. Yang P., Duan Y., Zhang P., Li Z., Wang C., Dong M., et al. Multiple-clade H5N1 influenza split vaccine elicits broad cross protection against lethal influenza virus challenge in mice by intranasal vaccination. PLoS ONE 2012, 7:e30252.
27. Huber V.C., Thomas P.G., McCullers J.A. A multi-valent vaccine approach that elicits broad immunity within an influenza subtype. Vaccine 2009, 27:1192-1200.
28. Laddy D.J., Yan J., Corbitt N., Kobasa D., Kobinger G.P., Weiner D.B. Immunogenicity of novel consensus-based DNA vaccines against avian influenza. Vaccine 2007, 25:2984-2989.
29. Laddy D.J., Yan J., Khan A.S., Andersen H., Cohn A., Greenhouse J., et al. Electroporation of synthetic DNA antigens offers protection in nonhuman primates challenged with highly pathogenic avian influenza virus. J Virol 2009, 83:4624-4630.
30. Laddy D.J., Yan J., Kutzler M., Kobasa D., Kobinger G.P., Khan A.S., et al. Heterosubtypic protection against pathogenic human and avian influenza viruses via in vivo electroporation of synthetic consensus DNA antigens. PLoS ONE 2008, 3:e2517.
31. Giles B.M., Ross T.M. A computationally optimized broadly reactive antigen (COBRA) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets. Vaccine 2011, 29:3043-3054.
32. Ducatez M.F., Bahl J., Griffin Y., Stigger-Rosser E., Franks J., Barman S., et al. Feasibility of reconstructed ancestral H5N1 influenza viruses for cross-clade protective vaccine development. Proc Natl Acad Sci USA 2011, 108:349-354.
33. Cattoli G., Milani A., Temperton N., Zecchin B., Buratin A., Molesti E., et al. Antigenic drift in H5N1 avian influenza virus in poultry is driven by mutations in major antigenic sites of the hemagglutinin molecule analogous to those for human influenza virus. J Virol 2011, 85:8718-8724.
34. Chen J.R., Yu Y.H., Tseng Y.C., Chiang W.L., Chiang M.F., Ko Y.A., et al. Vaccination of monoglycosylated hemagglutinin induces cross-strain protection against influenza virus infections. Proc Natl Acad Sci USA 2014, 111:2476-2481.
35. Das S.R., Hensley S.E., David A., Schmidt L., Gibbs J.S., Puigbo P., et al. Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc Natl Acad Sci USA 2011, 108:E1417-E1422.
36. Das S.R., Puigbo P., Hensley S.E., Hurt D.E., Bennink J.R., Yewdell J.W. Glycosylation focuses sequence variation in the influenza A virus H1 hemagglutinin globular domain. PLoS Pathog 2010, 6:e1001211.
37. Eggink D., Goff P.H., Palese P. Guiding the immune response against influenza virus hemagglutinin toward the conserved stalk domain by hyperglycosylation of the globular head domain. J Virol 2014, 88:699-704.
38. Kaverin N.V., Rudneva I.A., Govorkova E.A., Timofeeva T.A., Shilov A.A., Kochergin-Nikitsky K.S., et al. Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J Virol 2007, 81:12911-12917.
39. Kobayashi Y., Suzuki Y. Evidence for N-glycan shielding of antigenic sites during evolution of human influenza A virus hemagglutinin. J Virol 2012, 86:3446-3451.
40. Medina R.A., Stertz S., Manicassamy B., Zimmermann P., Sun X., Albrecht R.A., et al. Glycosylations in the globular head of the hemagglutinin protein modulate the virulence and antigenic properties of the H1N1 influenza viruses. Sci Transl Med 2013, 5:187ra70.
41. Wei C.J., Boyington J.C., Dai K., Houser K.V., Pearce M.B., Kong W.P., et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci Transl Med 2010, 2:24ra21.
42. Liu M., Wood J.M., Ellis T., Krauss S., Seiler P., Johnson C., et al. Preparation of a standardized, efficacious agricultural H5N3 vaccine by reverse genetics. Virology 2003, 314:580-590.
43. Lee C.W., Senne D.A., Suarez D.L. Generation of reassortant influenza vaccines by reverse genetics that allows utilization of a DIVA (Differentiating Infected from Vaccinated Animals) strategy for the control of avian influenza. Vaccine 2004, 22:3175-3181.
44. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Gao P., et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 1999, 96:9345-9350.
45. OIE (Office International des Epizooties) Avian influenza. Manual of standards for diagnostic tests and vaccines for terrestrial animals 2008, 465-481. Office International des Epizooties, Paris, France. 6th ed.
46. Ali A., Daniels J.B., Zhang Y., Rodriguez-Palacios A., Hayes-Ozello K., Mathes L., et al. Pandemic and seasonal human influenza virus infections in domestic cats: prevalence, association with respiratory disease, and seasonality patterns. J Clin Microbiol 2011, 49:4101-4105.
47. Archetti I., Horsfall F.L. Persistent antigenic variation of influenza A viruses after incomplete neutralization in ovo with heterologous immune serum. J Exp Med 1950, 92:441-462.
48. Cai Z., Zhang T., Wan X.F. A computational framework for influenza antigenic cartography. PLoS Comput Biol 2010, 16:e1000949.
49. Watanabe Y., Ibrahim M.S., Ellakany H.F., Kawashita N., Mizuike R., Hiramatsu H., et al. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog 2011, 7:e1002068.
50. Wang W., Lu B., Zhou H., Suguitan A.L., Cheng X., Subbarao K., et al. Glycosylation at 158N of the hemagglutinin protein and receptor binding specificity synergistically affect the antigenicity and immunogenicity of a live attenuated H5N1 A/Vietnam/1203/2004 vaccine virus in ferrets. J Virol 2010, 84:6570-6577.
51. Cai Z., Ducatez M.F., Yang J., Zhang T., Long L.P., Boon A.C., et al. Identifying antigenicity-associated sites in highly pathogenic H5N1 influenza virus hemagglutinin by using sparse learning. J Mol Biol 2012, 422:145-155.
52. Wang C.C., Chen J.R., Tseng Y.C., Hsu C.H., Hung Y.F., Chen S.W., et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci USA 2009, 106:18137-18142.
53. Yen H.L., Aldridge J.R., Boon A.C., Ilyushina N.A., Salomon R., Hulse-Post D.J., et al. Changes in H5N1 influenza virus hemagglutinin receptor binding domain affect systemic spread. Proc Natl Acad Sci USA 2009, 106:286-291.
54. Chen W., Sun S., Li Z. Two glycosylation sites in H5N1 influenza virus hemagglutinin that affect binding preference by computer-based analysis. PLoS ONE 2012, 7:e38794.
55. Duvvuri V.R., Duvvuri B., Cuff W.R., Wu G.E., Wu J. Role of positive selection pressure on the evolution of H5N1 hemagglutinin. Genomics Proteomics Bioinf 2009, 7:47-56.
56. Peng Y., Zou Y., Li H., Li K., Jiang T. Inferring the antigenic epitopes for highly pathogenic avian influenza H5N1 viruses. Vaccine 2014, 32:671-676.
57. Hensley S.E., Das S.R., Bailey A.L., Schmidt L.M., Hickman H.D., Jayaraman A., et al. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 2009, 326:734-736.
58. Arafa A., Suarez D., Kholosy S.G., Hassan M.K., Nasef S., Selim A., et al. Evolution of highly pathogenic avian influenza H5N1 viruses in Egypt indicating progressive adaptation. Arch Virol 2012, 157:1931-1947.