Protective immunity against H5N1 influenza virus by a single dose vaccination with virus-like particles

Virology

Volumn 405, Issue 1, 2010, Pages 165-175

  Song, Jae Min ^a   Hossain, Jaber ^b   Yoo, Dae Goon ^a   Lipatov, Aleksandr S ^b   Davis, C Todd ^b   Quan, Fu Shi ^a   Chen, Li Mei ^b   Hogan, Robert J ^c   Donis, Ruben O ^b   Compans, Richard W ^a   Kang, Sang Moo ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

H5N1; Influenza virus; Memory immune responses; Protection; Subunit vaccine; Virus like particles

Indexed keywords

H5 VLP INFLUENZA VACCINE; HEMAGGLUTININ; INFLUENZA VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DETERMINATION; DRUG EFFICACY; DRUG SCREENING; DRUG SYNTHESIS; FEMALE; GENE DELETION; IMMUNOGENICITY; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN MOTIF; SINGLE DRUG DOSE; TH1 CELL; VACCINATION; VIRUS PARTICLE; WILD TYPE;

ORTHOMYXOVIRIDAE;

EID: 77955511874     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.05.034     Document Type: Article

References (63)

1. Atmar R.L., Keitel W.A., Patel S.M., Katz J.M., She D., El Sahly H., Pompey J. Safety and immunogenicity of nonadjuvanted and MF59-adjuvanted influenza A/H9N2 vaccine preparations. Clin Infect Dis 2006, 43(9):1135-1142.
2. Bachmann M.F., Zinkernagel R.M. The influence of virus structure on antibody responses and virus serotype formation. Immunol. Today 1996, 17(12):553-558.
3. Bachmann M.F., Zinkernagel R.M., Oxenius A. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 1998, 161(11):5791-5794.
4. Bot A., Bot S., Bona C., Bona C., Cate T.R., Couch R.B. Protective role of gamma interferon during the recall response to influenza virus. J. Virol. 1998, 72(8):6637-6645.
5. Bresson J.L., Perronne C., Launay O., Gerdil C., Saville M., Wood J., Hoschler K., Zambon M.C. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 2006, 367(9523):1657-1664.
6. Bright R.A., Carter D.M., Crevar C.J., Toapanta F.R., Steckbeck J.D., Cole K.S., Kumar N.M., Pushko P., Smith G., Tumpey T.M., Ross T.M. 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.
7. Bright R.A., Carter D.M., Daniluk S., Toapanta F.R., Ahmad A., Gavrilov V., Massare M., Pushko P., Mytle N., Rowe T., Smith G., Ross T.M. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007, 25(19):3871-3878.
8. Cheung C.L., Rayner J.M., Smith G.J., Wang P., Naipospos T.S., Zhang J., Yuen K.Y., Webster R.G., Peiris J.S., Guan Y., Chen H. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J. Infect. Dis. 2006, 193(12):1626-1629.
9. Claas E.C., Osterhaus A.D., van Beek R., De Jong J.C., Rimmelzwaan G.F., Senne D.A., Krauss S., Shortridge K.F., Webster R.G. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998, 351(9101):472-477.
10. Coutelier J.P., van der Logt J.T., Heessen F.W., Warnier G., Van Snick J. IgG2a restriction of murine antibodies elicited by viral infections. J. Exp. Med. 1987, 165(1):64-69.
11. Crotty S., Felgner P., Davies H., Glidewell J., Villarreal L., Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 2003, 171(10):4969-4973.
12. de Jong M.D., Tran T.T., Truong H.K., Vo M.H., Smith G.J., Nguyen V.C., Bach V.C., Phan T.Q., Do Q.H., Guan Y., Peiris J.S., Tran T.H., Farrar J. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J. Med. 2005, 353(25):2667-2672.
13. Donis R.O. Evolution of H5N1 avian influenza viruses in Asia. Emerg. Infect. Dis. 2005, 11(10):1515-1521.
14. Fazekas G., Rosenwirth B., Dukor P., Gergely J., Rajnavolgyi E. IgG isotype distribution of local and systemic immune responses induced by influenza virus infection. Eur. J. Immunol. 1994, 24(12):3063-3067.
15. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., Rimmelzwaan G.F., Olsen B., Osterhaus A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79(5):2814-2822.
16. Fouchier R.A., Schneeberger P.M., Rozendaal F.W., Broekman J.M., Kemink S.A., Munster V., Kuiken T., Rimmelzwaan G.F., Schutten M., Van Doornum G.J., Koch G., Bosman A., Koopmans M., Osterhaus A.D. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Nat. Acad. Sci. U.S.A. 2004, 101(5):1356-1361.
17. Gessner J.E., Heiken H., Tamm A., Schmidt R.E. The IgG Fc receptor family. Ann. Hematol. 1998, 76(6):231-248.
18. Gillim-Ross L., Subbarao K. Emerging respiratory viruses: challenges and vaccine strategies. Clin. Microbiol. Rev. 2006, 19(4):614-636.
19. Govorkova E.A., Webby R.J., Humberd J., Seiler J.P., Webster R.G. Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. J. Infect. Dis. 2006, 194(2):159-167.
20. Haynes J.R., Dokken L., Wiley J.A., Cawthon A.G., Bigger J., Harmsen A.G., Richardson C. Influenza-pseudotyped Gag virus-like particle vaccines provide broad protection against highly pathogenic avian influenza challenge. Vaccine 2009, 27(4):530-541.
21. Hehme N., Engelmann H., Kunzel W., Neumeier E., Sanger R. Pandemic preparedness: lessons learnt from H2N2 and H9N2 candidate vaccines. Med. Microbiol. Immunol. 2002, 191(3-4):203-208.
22. Heusser C.H., Anderson C.L., Grey H.M. Receptors for IgG: subclass specificity of receptors on different mouse cell types and the definition of two distinct receptors on a macrophage cell line. J. Exp. Med. 1977, 145(5):1316-1327.
23. Huber V.C., Lynch J.M., Bucher D.J., Le J., Metzger D.W. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 2001, 166(12):7381-7388.
24. Huber V.C., McKeon R.M., Brackin M.N., Miller L.A., Keating R., Brown S.A., Makarova N., Perez D.R., Macdonald G.H., McCullers J.A. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin. Vaccine Immunol. 2006, 13(9):981-990.
25. Jayasekera J.P., Moseman E.A., Carroll M.C. Natural antibody and complement mediate neutralization of influenza virus in the absence of prior immunity. J. Virol. 2007, 81(7):3487-3494.
26. Kalia V., Sarkar S., Gourley T.S., Rouse B.T., Ahmed R. Differentiation of memory B and T cells. Curr. Opin. Immunol. 2006, 18(3):255-264.
27. Kang S.M., Yoo D.G., Lipatov A.S., Song J.M., Davis C.T., Quan F.S., Chen L.M., Donis R.O., Compans R.W. Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS ONE 2009, 4(3):e4667.
28. Le Q.M., Kiso M., Someya K., Sakai Y.T., Nguyen T.H., Nguyen K.H., Pham N.D., Ngyen H.H., Yamada S., Muramoto Y., Horimoto T., Takada A., Goto H., Suzuki T., Suzuki Y., Kawaoka Y. Avian flu: isolation of drug-resistant H5N1 virus. Nature 2005, 437(7062):1108.
29. Lin J., Zhang J., Dong X., Fang H., Chen J., Su N., Gao Q., Zhang Z., Liu Y., Wang Z., Yang M., Sun R., Li C., Lin S., Ji M., Liu Y., Wang X., Wood J., Feng Z., Wang Y., Yin W. Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 2006, 368(9540):991-997.
30. Lipatov A.S., Hoffmann E., Salomon R., Yen H.L., Webster R.G. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J. Infect. Dis. 2006, 194(8):1040-1043.
31. Moran T.M., Park H., Fernandez-Sesma A., Schulman J.L. Th2 responses to inactivated influenza virus can Be converted to Th1 responses and facilitate recovery from heterosubtypic virus infection. J. Infect. Dis. 1999, 180(3):579-585.
32. Mozdzanowska K., Feng J., Eid M., Zharikova D., Gerhard W. Enhancement of neutralizing activity of influenza virus-specific antibodies by serum components. Virology 2006, 352(2):418-426.
33. Nava G.M., Attene-Ramos M.S., Ang J.K., Escorcia M. Origins of the new influenza A(H1N1) virus: time to take action. Euro Surveill. 2009, 14(22).
34. Neuberger M.S., Rajewsky K. Activation of mouse complement by monoclonal mouse antibodies. Eur. J. Immunol. 1981, 11(12):1012-1016.
35. Nicholson K.G., Colegate A.E., Podda A., Stephenson I., Wood J., Ypma E., Zambon M.C. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. Lancet 2001, 357(9272):1937-1943.
36. Nicholson K.G., Tyrrell D.A., Harrison P., Potter C.W., Jennings R., Clark A., Schild G.C., Wood J.M., Yetts R., Seagroatt V., Huggins A., Anderson S.G. Clinical studies of monovalent inactivated whole virus and subunit A/USSR/77 (H1N1) vaccine: serological responses and clinical reactions. J. Biol. Stand. 1979, 7(2):123-136.
37. 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 2005, 23(22):2943-2952.
38. Peiris M., Yuen K.Y., Leung C.W., Chan K.H., Ip P.L., Lai R.W., Orr W.K., Shortridge K.F. Human infection with influenza H9N2. Lancet 1999, 354(9182):916-917.
39. Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol. Rev. 2004, 199:227-250.
40. Pulendran B., Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006, 124(4):849-863.
41. Quan F.S., Huang C., Compans R.W., Kang S.M. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol. 2007, 81(7):3514-3524.
42. Rohm C., Zhou N., Suss J., Mackenzie J., Webster R.G. Characterization of a novel influenza hemagglutinin, H15: criteria for determination of influenza A subtypes. Virology 1996, 217(2):508-516.
43. Slifka M.K., Ahmed R. Limiting dilution analysis of virus-specific memory B cells by an ELISPOT assay. J. Immunol. Meth. 1996, 199(1):37-46.
44. Slifka M.K., Antia R., Whitmire J.K., Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity 1998, 8(3):363-372.
45. Slifka M.K., Matloubian M., Ahmed R. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 1995, 69(3):1895-1902.
46. Solovyov A., Palacios G., Briese T., Lipkin W.I., Rabadan R. Cluster analysis of the origins of the new influenza A(H1N1) virus. Euro Surveill. 2009, 14(21).
47. Steinhauer D.A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 1999, 258(1):1-20.
48. Stephenson I., Nicholson K.G., Gluck R., Mischler R., Newman R.W., Palache A.M., Verlander N.Q., Warburton F., Wood J.M., Zambon M.C. Safety and antigenicity of whole virus and subunit influenza A/Hong Kong/1073/99 (H9N2) vaccine in healthy adults: phase I randomised trial. Lancet 2003, 362(9400):1959-1966.
49. Stieneke-Grober A., Vey M., Angliker H., Shaw E., Thomas G., Roberts C., Klenk H.D., Garten W. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 1992, 11(7):2407-2414.
50. Subbarao K., Chen H., Swayne D., Mingay L., Fodor E., Brownlee G., Xu X., Lu X., Katz J., Cox N., Matsuoka Y. Evaluation of a genetically modified reassortant H5N1 influenza A virus vaccine candidate generated by plasmid-based reverse genetics. Virology 2003, 305(1):192-200.
51. Subbarao K., Joseph T. Scientific barriers to developing vaccines against avian influenza viruses. Nat. Rev. Immunol. 2007, 7(4):267-278.
52. Subbarao K., Klimov A., Katz J., Regnery H., Lim W., Hall H., Perdue M., Swayne D., Bender C., Huang J., Hemphill M., Rowe T., Shaw M., Xu X., Fukuda K., Cox N. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998, 279(5349):393-396.
53. Sui J., Hwang W.C., Perez S., Wei G., Aird D., Chen L.M., Santelli E., Stec B., Cadwell G., Ali M., Wan H., Murakami A., Yammanuru A., Han T., Cox N.J., Bankston L.A., Donis R.O., Liddington R.C., Marasco W.A. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 2009, 16(3):265-273.
54. Swain S.L., Agrewala J.N., Brown D.M., Jelley-Gibbs D.M., Golech S., Huston G., Jones S.C., Kamperschroer C., Lee W.H., McKinstry K.K., Roman E., Strutt T., Weng N.P. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol. Rev. 2006, 211:8-22.
55. Thomas P.G., Brown S.A., Yue W., So J., Webby R.J., Doherty P.C. An unexpected antibody response to an engineered influenza virus modifies CD8+ T cell responses. Proc. Nat. Acad. Sci. U.S.A. 2006, 103(8):2764-2769.
56. Treanor J.J., Campbell J.D., Zangwill K.M., Rowe T., Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J. Med. 2006, 354(13):1343-1351.
57. Treanor J.J., Wilkinson B.E., Masseoud F., Hu-Primmer J., Battaglia R., O'Brien D., Wolff M., Rabinovich G., Blackwelder W., Katz J.M. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine 2001, 19(13-14):1732-1737.
58. Wakamiya N., Okuno Y., Sasao F., Ueda S., Yoshimatsu K., Naiki M., Kurimura T. Isolation and characterization of conglutinin as an influenza A virus inhibitor. Biochem. Biophys. Res. Commun. 1992, 187(3):1270-1278.
59. Wan X.F., Nguyen T., Davis C.T., Smith C.B., Zhao Z.M., Carrel M., Inui K., Do H.T., Mai D.T., Jadhao S., Balish A., Shu B., Luo F., Emch M., Matsuoka Y., Lindstrom S.E., Cox N.J., Nguyen C.V., Klimov A., Donis R.O. Evolution of highly pathogenic H5N1 avian influenza viruses in Vietnam between 2001 and 2007. PLoS ONE 2008, 3(10):e3462.
60. Webby R.J., Perez D.R., Coleman J.S., Guan Y., Knight J.H., Govorkova E.A., McClain-Moss L.R., Peiris J.S., Rehg J.E., Tuomanen E.I., Webster R.G. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 2004, 363(9415):1099-1103.
61. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56(1):152-179.
62. Wong S.S., Yuen K.Y. Avian influenza virus infections in humans. Chest 2006, 129(1):156-168.
63. Wright P.F., Thompson J., Vaughn W.K., Folland D.S., Sell S.H., Karzon D.T. Trials of influenza A/New Jersey/76 virus vaccine in normal children: an overview of age-related antigenicity and reactogenicity. J. Infect. Dis. 1977, 136(Suppl):S731-S741.