A computationally optimized broadly reactive antigen (COBRA) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets

Vaccine

Volumn 29, Issue 16, 2011, Pages 3043-3054

  Giles, Brendan M ^a   Ross, Ted M ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

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

Author keywords

Consensus; H5N1; Influenza; Vaccine; Virus like particles

Indexed keywords

COMPUTATIONALLY OPTIMIZED BROADLY REACTIVE ANTIGEN HEMAGGLUTININ; CROSS REACTING ANTIBODY; HEMAGGLUTININ; INFLUENZA VACCINE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; FEMALE; FERRET; HUMAN; HUMAN CELL; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SEROCONVERSION; VACCINATION; VIRUS LIKE AGENT;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIGENS, VIRAL; COMPUTATIONAL BIOLOGY; COMPUTER-AIDED DESIGN; DOGS; DRUG DESIGN; FEMALE; FERRETS; HEK293 CELLS; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; PLAQUE ASSAY; TRANSFECTION;

EID: 79953244722     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.01.100     Document Type: Article

References (67)

1. World Health Organization. Avian influenza: assessing the pandemic threat. Available from: http://www.who.int/csr/disease/influenza/WHO_CDS_2005_29/en/index.html; 2005.
2. World Health Organization. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. Available from: http://www.who.int/csr/disease/avian_influenza/country/cases_table_2008_ 02_26/en/index.html; 2008.
3. Li K.S., Guan Y., Wang J., Smith G.J.D., Xu K.M., Duan L., et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004, 430(6996):209-213.
4. Chen L.-M., Davis C.T., Zhou H., Cox N.J., Donis R.O. Genetic compatibility and virulence of reassortants derived from contemporary avian H5N1 and human H3N2 influenza A viruses. PLoS Pathogens 2008, 4(5):e1000072.
5. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S, Neumann G, et al. Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proceedings of the National Academic of Science 2010;107(10):4687-92.
6. Octaviani CP, Ozawa M, Yamada S, Goto H, Kawaoka Y. High level of genetic compatibility between swine-origin H1N1 and highly pathogenic avian H5N1 influenza viruses. The Journal of Virology 2010;84(20):10918-22.
7. World Health Organization. Antigenic and genetic characteristics of H5N1 viruses and candidate H5N1 vaccine viruses developed for potential use as human vaccines. Available from: http://www.who.int/csr/disease/avian_influenza/guidelines/H5VaccineVirus Update20080214.pdf; February 2008 [accessed 27.02.08].
8. Wang J., Vijaykrishna D., Duan L., Bahl J., Zhang J.X., Webster R.G., et al. Identification of the progenitors of Indonesian and vietnamese avian influenza A (H5N1) viruses from Southern China. The Journal of Virology 2008, 82(7):3405-3414.
9. Webster R.G., Govorkova E.A. H5N1 influenza-continuing evolution and spread. The New England Journal of Medicine 2006, 355(21):2174-2177.
10. Prabakaran M, He F, Meng T, Madhan S, Yunrui T, Jia Q, et al. Neutralizing epitopes of influenza virus hemagglutinin: target for the development of a universal vaccine against H5N1 lineages. The Journal of Virology 2010;84(22):11822-30.
11. Tompkins S.M., Zhao Z.-S., Lo C.-Y., Misplon J.A., Liu T., Ye Z., et al. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerging Infectious Diseases 2007, 13(March (3)):426-435.
12. Kodihalli S., Kobasa D.L., Webster R.G. Strategies for inducing protection against avian influenza A virus subtypes with DNA vaccines. Vaccine 2000, 18(23):2592-2599.
13. Bianchi E., Liang X., Ingallinella P., Finotto M., Chastain M.A., Fan J., et al. Universal influenza B vaccine based on the maturational cleavage site of the hemagglutinin precursor. The Journal of Virology 2005, 79(12):7380-7388.
14. Steel J., Lowen A.C., Wang T.T., Yondola M., Gao Q., Haye K., et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 2010, 1(1). pp. e00018-10.
15. 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(16):2984-2989.
16. 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(6):e2517.
17. 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. The Journal of Virology 2009, 83(9):4624-4630.
18. Chen M.-W., Cheng T-JR, Huang Y., Jan J.-T., Ma S.-H., Yu A.L., et al. A consensus hemagglutinin-based DNA vaccine that protects mice against divergent H5N1 influenza viruses. Proceedings of the National Academy of Sciences 2008, 105(36):13538-13543.
19. McBurney S.P., Ross T.M. Human immunodeficiency virus-like particles with consensus envelopes elicited broader cell-mediated peripheral and mucosal immune responses than polyvalent and monovalent Env vaccines. Vaccine 2009, 27(32):4337-4349.
20. Weaver E.A., Lu Z., Camacho Z.T., Moukdar F., Liao H.-X., Ma B.-J., et al. Cross-subtype T-cell immune responses induced by a human immunodeficiency virus type 1 group M consensus Env immunogen. The Journal of Virology 2006, 80(14):6745-6756.
21. Yan J, Yoon H, Kumar S, Ramanathan MP, Corbitt N, Kutzler M, et al. Enhanced cellular immune responses elicited by an engineered HIV-1 subtype B consensus-based envelope DNA vaccine. Molecular Therapy; 15(2):411-21.
22. Bao Y., Bolotov P., Dernovoy D., Kiryutin B., Zaslavsky L., Tatusova T., et al. The influenza virus resource at the national center for biotechnology information. The Journal of Virology 2008, 82(2):596-601.
23. Wu C-Y, Yeh Y-C, Yang Y-C, Chou C, Liu M-T, Wu H-S, et al. Mammalian expression of virus-like particles for advanced mimicry of authentic influenza virus. PLoS ONE 2010;5(3):e9784.
24. Garland S.M., Hernandez-Avila M., Wheeler C.M., Perez G., Harper D.M., Leodolter S., et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. New England Journal of Medicine 2007, 356(19):1928-1943.
25. Bright R.A., Carter D.M., Crevar C.J., Toapanta F.R., Steckbeck J.D., Cole K.S., et al. Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle. PLoS ONE 2008, 3(1):e1501.
26. Yang Z.-y., Chakrabarti B.K., Xu L., Welcher B., Kong W-p, Leung K., et al. Selective modification of variable loops alters tropism and enhances immunogenicity of human immunodeficiency virus type 1 envelope. The Journal of Virology 2004, 78(8):4029-4036.
27. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics International 2004, 11(7):36-42.
28. Toapanta F., Ross T. Impaired immune responses in the lungs of aged mice following influenza infection. Respiratory Research 2009, 10(1):112.
29. Gillim-Ross L., Subbarao K. Emerging respiratory viruses: challenges and vaccine strategies. Clinical Microbiology Reviews 2006, 19(October (4)):614-636.
30. Bright R.A., Medina M.J., Xu X., Perez-Oronoz G., Wallis T.R., Davis X.M., et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 2005 Oct 1, 366(9492):1175-1181.
31. Bright R.A., Ross T.M., Subbarao K., Robinson H.L., Katz J.M. Impact of glycosylation on the immunogenicity of a DNA-based influenza H5 HA vaccine. Virology 2003, 308(April (2)):270-278.
32. Bright R.A., Shay D.K., Shu B., Cox N.J., Klimov A.I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 2006, 295(February (8)):891-894.
33. Mitchell J.A., Green T.D., Bright R.A., Ross T.M. Induction of heterosubtypic immunity to influenza A virus using a DNA vaccine expressing hemagglutinin-C3d fusion proteins. Vaccine 2003, 21(February (9-10)):902-914.
34. Ross T.M., Xu Y., Bright R.A., Robinson H.L. C3d enhancement of antibodies to hemagglutinin accelerates protection against influenza virus challenge. Nature Immunology 2000, 1(2):127-131.
35. Askonas B., McMichael A., Webster R. The immune response to influenza viruses and the problem of protection against infection. Bascin and applied influenza research 1982, 159-188. CRC Press. A. Beare (Ed.).
36. Nefkens G., Ling L., Nicholls T., et al. Hemagglutinin pseudotyped lentiviral particles: characterization of a new method for avian H5N1 influenza sero-diagnosis. Journal of Clinical Virology 2007, 39(1):27-33.
37. Haynes J.R., Dokken L., Wiley J.A., Cawthon A.G., Bigger J., Harmsen A.G., et al. Influenza-pseudotyped Gag virus-like particle vaccines provide broad protection against highly pathogenic avian influenza challenge. Vaccine 2009, 27(4):530-541.
38. Kesturu G.S., Colleton B.A., Liu Y., Heath L., Shaikh O.S., Rinaldo J.C.R., et al. Minimization of genetic distances by the consensus, ancestral, and center-of-tree (COT) sequences for HIV-1 variants within an infected individual and the design of reagents to test immune reactivity. Virology 2006, 348(2):437-448.
39. Nickle D.C., Jensen M.A., Gottlieb G.S., Shriner D., Learn G.H., Rodrigo A.G., et al. Consensus and ancestral state HIV vaccines. Science 2003, 299(5612):1515c-1518c.
40. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 2007, 24(8):1586-1591.
41. Gao F., Liao H.-X., Hahn B.H., Letvin N.L., Korber B.T., Haynes B.F. Centralized HIV-1 envelope immunogens and neutralizing antibodies. Current HIV Research 2007, 5(6):572-577.
42. Ducatez MF, 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. Proceedings of the National Academy of Sciences 2011;108(1):349-54.
43. Gao F., Weaver E.A., Lu Z., Li Y., Liao H.-X., Ma B., et al. Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group M consensus envelope glycoprotein. The Journal of Virology 2005, 79(2):1154-1163.
44. Hamano T., Sawanpanyalert P., Yanai H., Piyaworawong S., Hara T., Sapsutthipas S., et al. Determination of HIV Type 1 CRF01_AE gag p17 and env-V3 consensus sequences for HIV/AIDS vaccine design. AIDS Research and Human Retroviruses 2004, 20(3):337-340.
45. Krohn K., Stanescu I., Blazevic V., Vesikari T., Ranki A., Ustav M. A DNA HIV-1 vaccine based on a fusion gene expressing non-structural and structural genes of consensus sequence of the A-C subtypes and the ancestor sequence of the F-H subtypes. Preclinical and clinical studies. Microbes and Infection 2005, 7(14):1405-1413.
46. Mwau M., Cebere I., Sutton J., Chikoti P., Winstone N., Wee E.G.T., et al. A human immunodeficiency virus 1 (HIV-1) clade A vaccine in clinical trials: stimulation of HIV-specific T-cell responses by DNA and recombinant modified vaccinia virus Ankara (MVA) vaccines in humans. Journal of General Virology 2004, 85(4):911-919.
47. Malm M., Rollman E., Ustav M., Hinkula J., Krohn K., Wahren B., et al. Cross-clade protection induced by human immunodeficiency virus-1 DNA immunogens expressing consensus sequences of multiple genes and epitopes from subtypes A, B, C, and FGH. Viral Immunology 2005, 18(4):678-688.
48. Bright R.A., Carter D.M., Daniluk S., Toapanta F.R., Ahmad A., Gavrilov V., et al. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007, 25(19):3871-3878.
49. Mahmood K., Bright R., Mytle N., Carter D., Crevar C., Achenbach J., et al. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine 2008, 26:5393-5399.
50. Subbarao K., Joseph T. Scientific barriers to developing vaccines against avian influenza viruses. Nature Reviews. Immunology 2007, 7(4):267-278.
51. Young K.R., Ross T.M. Particle-based vaccines for HIV-1 Infection. Current Drug Targets. Infectious Disorders 2003, 3:151-169.
52. Huber V.C., McKeon R.M., Brackin M.N., Miller L.A., Keating R., Brown S.A., et al. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clinical and Vaccine Immunology 2006, 13(9):981-990.
53. Janeway C.A., Medzhitov R. Innate immune recognition. Annual Review of Immunology 2002, 20(1):197-216.
54. Tritto E., Mosca F., De Gregorio E. Mechanism of action of licensed vaccine adjuvants. Vaccine 2009, 27(25-26):3331-3334.
55. Eisenbarth S.C., Colegio O.R., O'Connor W., Sutterwala F.S., Flavell R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008, 453(7198):1122-1126.
56. Govorkova E., Webby R., Humberd J., Seiler J., Webster R. Immunization with reverse genetics produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. The Journal of Infectious Diseases 2006, 194(2):159-167.
57. Ninomiya A., Imai M., Tashiro M., Odagiri T. Inactivated influenza H5N1 whole-virus vaccine with aluminum adjuvant induces homologous and heterologous protective immunities against lethal challenge with highly pathogenic H5N1 avian influenza viruses in a mouse model. Vaccine 2007, 25(18):3554-3560.
58. Lipatov A., Hoffmann E., Salomon R., Yen H.-L., Webster R. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/vietnam/1203/04(H5N1) virus in ferrets. The Journal of Infectious Diseases 2006, 194(8):1040-1043.
59. Suguitan A.L., McAuliffe J., Mills K.L., Jin H., Duke G., Lu B., et al. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Medicine 2006, 3(9):e360.
60. Lu X., Edwards L.E., Desheva J.A., Nguyen D.C., Rekstin A., Stephenson I., et al. Cross-protective immunity in mice induced by live-attenuated or inactivated vaccines against highly pathogenic influenza A (H5N1) viruses. Vaccine 2006, 24(44-46):6588-6593.
61. Hoelscher M.A., Garg S., Bangari D.S., Belser J.A., Lu X., Stephenson I., et al. Development of adenoviral-vector-based pandemic influenza vaccine against antigenically distinct human H5N1 strains in mice. The Lancet 2006, 367(9509):475-481.
62. Davenport F. Control of influenza. Medical Journal of Australia 1973, (Suppl.):33-38.
63. Chen Z., Kadowaki S-e, Hagiwara Y., Yoshikawa T., Matsuo K., Kurata T., et al. Cross-protection against a lethal influenza virus infection by DNA vaccine to neuraminidase. Vaccine 2000, 18(28):3214-3222.
64. Sandbulte M.R., Jimenez G.S., Boon A.C.M., Smith L.R., Treanor J.J., Webby R.J. Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Medicine 2007, 4(2):e59.
65. Kreijtz J.H.C.M., Bodewes R., van Amerongen G., Kuiken T., Fouchier R.A.M., Osterhaus A.D.M.E., et al. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 2007, 25(4):612-620.
66. Furuya Y, Chan J, Regner M, Lobigs M, Koskinen A, Kok T, et al. Cytotoxic T cells are the predominant players providing cross-protective immunity induced by γ-irradiated influenza A viruses. The Journal of Virology 2010;84(9):4212-21.
67. Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, Salimi N, et al. The immune epitope database 2.0. Nucleic Acids Research 2009;38(Suppl. 1):D854-62.