Immunogenicity of low-pH treated whole viral influenza vaccine

Virology

Volumn 417, Issue 1, 2011, Pages 196-202

  Quan, Fu Shi ^a   Li, Zhu Nan ^a,b   Kim, Min Chul ^a   Yang, Dan ^a   Compans, Richard W ^a   Steinhauer, David A ^a   Kang, Sang Moo ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c NONE   (United States)

Author keywords

Conformational change; Immunogenicity; Influenza; Low pH; Vaccine

Indexed keywords

INACTIVATED VIRUS VACCINE; INFLUENZA VACCINE; VIRUS HEMAGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ANTIGENICITY; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS REACTION; DRUG EFFICACY; DRUG FORMULATION; DRUG STABILITY; FEMALE; HEMAGGLUTINATION TEST; IMMUNIZATION; IMMUNOGENICITY; IMMUNOREACTIVITY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CLEAVAGE; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; CELL LINE; CROSS REACTIONS; DOGS; FEMALE; HEMAGGLUTININS; HYDROGEN-ION CONCENTRATION; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN CONFORMATION; VACCINES, INACTIVATED;

MUS; ORTHOMYXOVIRIDAE;

EID: 79960943055     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.05.014     Document Type: Article

References (38)

1. Bizebard T., Gigant B., Rigolet P., Rasmussen B., Diat O., Bosecke P., Wharton S.A., Skehel J.J., Knossow M. Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 1995, 376(6535):92-94.
2. Bommakanti G., Citron M.P., Hepler R.W., Callahan C., Heidecker G.J., Najar T.A., Lu X., Joyce J.G., Shiver J.W., Casimiro D.R., ter Meulen J., Liang X., Varadarajan R. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(31):13701-13706.
3. Bullough P.A., Hughson F.M., Skehel J.J., Wiley D.C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 1994, 371(6492):37-43.
4. Daniels R.S., Douglas A.R., Skehel J.J., Wiley D.C. Analyses of the antigenicity of influenza haemagglutinin at the pH optimum for virus-mediated membrane fusion. J. Gen. Virol. 1983, 64(Pt 8):1657-1662.
5. Ekiert D.C., Bhabha G., Elsliger M.A., Friesen R.H., Jongeneelen M., Throsby M., Goudsmit J., Wilson I.A. Antibody recognition of a highly conserved influenza virus epitope. Science 2009, 324(5924):246-251.
6. Gerhard W., Yewdell J., Frankel M.E., Webster R. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 1981, 290(5808):713-717.
7. Hashem A.M., Van Domselaar G., Li C., Wang J., She Y.M., Cyr T.D., Sui J., He R., Marasco W.A., Li X. Universal antibodies against the highly conserved influenza fusion peptide cross-neutralize several subtypes of influenza A virus. Biochem. Biophys. Res. Commun. 2010, 403(2):247-251.
8. Kim Y.C., Quan F.S., Compans R.W., Kang S.M., Prausnitz M.R. Formulation and coating of microneedles with inactivated influenza virus to improve vaccine stability and immunogenicity. J. Control. Release 2010, 142(2):187-195.
9. Klenk H.D., Rott R., Orlich M., Blodorn J. Activation of influenza A viruses by trypsin treatment. Virology 1975, 68(2):426-439.
10. Kostolansky F., Russ G., Mucha V., Styk B. Changes in the influenza virus haemagglutinin at acid pH detected by monoclonal antibodies to glycopolypeptides HA1 and HA2. Arch. Virol. 1988, 101(1-2):13-24.
11. Laver W.G., Gerhard W., Webster R.G., Frankel M.E., Air G.M. Antigenic drift in type A influenza virus: peptide mapping and antigenic analysis of A/PR/8/34 (HON1) variants selected with monoclonal antibodies. Proc. Natl. Acad. Sci. U.S.A. 1979, 76(3):1425-1429.
12. Laver W.G., Air G.M., Dopheide T.A., Ward C.W. Amino acid sequence changes in the haemagglutinin of A/Hong Kong (H3N2) influenza virus during the period 1968-77. Nature 1980, 283(5746):454-457.
13. Lazarowitz S.G., Choppin P.W. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 1975, 68(2):440-454.
14. Maeda T., Kawasaki K., Ohnishi S. Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus-induced hemolysis and fusion at pH 5.2. Proc. Natl. Acad. Sci. U.S.A. 1981, 78(7):4133-4137.
15. Prabhu N., Prabakaran M., Ho H.T., Velumani S., Qiang J., Goutama M., Kwang J. Monoclonal antibodies against the fusion peptide of hemagglutinin protect mice from lethal influenza A virus H5N1 infection. J. Virol. 2009, 83(6):2553-2562.
16. 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.
17. Quan F.S., Compans R.W., Nguyen H.H., Kang S.M. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol. 2008, 82(3):1350-1359.
18. Quan F.S., Kim Y.C., Yoo D.G., Compans R.W., Prausnitz M.R., Kang S.M. Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin. PLoS One 2009, 4(9):e7152.
19. Quan F.S., Kim Y.C., Vunnava A., Yoo D.G., Song J.M., Prausnitz M.R., Compans R.W., Kang S.M. Intradermal vaccination with influenza virus-like particles by using microneedles induces protection superior to that with intramuscular immunization. J. Virol. 2010, 84(15):7760-7769.
20. Ruigrok R.W., Aitken A., Calder L.J., Martin S.R., Skehel J.J., Wharton S.A., Weis W., Wiley D.C. Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J. Gen. Virol. 1988, 69(Pt 11):2785-2795.
21. Skehel J.J., Bayley P.M., Brown E.B., Martin S.R., Waterfield M.D., White J.M., Wilson I.A., Wiley D.C. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 1982, 79(4):968-972.
22. Skehel J.J., Bizebard T., Bullough P.A., Hughson F.M., Knossow M., Steinhauer D.A., Wharton S.A., Wiley D.C. Membrane fusion by influenza hemagglutinin. Cold Spring Harbor Symposia on Quantitative Biology 1995, 573-580. Cold Spring Harbor Laboratory Press, LX.
23. Song J.M., Wang B.Z., Park K.M., Van Rooijen N., Quan F.S., Kim M.C., Jin H.T., Pekosz A., Compans R.W., Kang S.M. Influenza virus-like particles containing M2 induce broadly cross protective immunity. PLoS One 2011, 6(1):e14538.
24. Stanekova Z., Kiraly J., Stropkovska A., Mikuskova T., Mucha V., Kostolansky F., Vareckova E. Heterosubtypic protective immunity against influenza A virus induced by fusion peptide of the hemagglutinin in comparison to ectodomain of M2 protein. Acta Virol. 2011, 55(1):61-67.
25. Steel J., Lowen A.C., Wang T., Yondola M., Gao Q., Haye K., Garcia-Sastre A., Palese P. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 2010, 1(1).
26. Steinhauer D.A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 1999, 258(1):1-20.
27. 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.
28. Vanlandschoot P., Beirnaert E., Barrere B., Calder L., Millar B., Wharton S., Jou W.M., Fiers W. An antibody which binds to the membrane-proximal end of influenza virus haemagglutinin (H3 subtype) inhibits the low-pH-induced conformational change and cell-cell fusion but does not neutralize virus. J. Gen. Virol. 1998, 79(Pt 7):1781-1791.
29. Wang T.T., Tan G.S., Hai R., Pica N., Ngai L., Ekiert D.C., Wilson I.A., Garcia-Sastre A., Moran T.M., Palese P. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(44):18979-18984.
30. Wang T.T., Tan G.S., Hai R., Pica N., Petersen E., Moran T.M., Palese P. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog. 2010, 6(2):e1000796.
31. Webster R.G., Brown L.E., Jackson D.C. Changes in the antigenicity of the hemagglutinin molecule of H3 influenza virus at acidic pH. Virology 1983, 126(2):587-599.
32. Wharton S.A., Calder L.J., Ruigrok R.W., Skehel J.J., Steinhauer D.A., Wiley D.C. Electron microscopy of antibody complexes of influenza virus haemagglutinin in the fusion pH conformation. EMBO J. 1995, 14(2):240-246.
33. White J., Kartenbeck J., Helenius A. Membrane fusion activity of influenza virus. EMBO J. 1982, 1(2):217-222.
34. Wiley D.C., Skehel J.J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 1987, 56:365-394.
35. Wiley D.C., Wilson I.A., Skehel J.J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981, 289(5796):373-378.
36. Wilson I.A., Skehel J.J., Wiley D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3A resolution. Nature 1981, 289(5796):366-373.
37. Yewdell J.W., Gerhard W., Bachi T. Monoclonal anti-hemagglutinin antibodies detect irreversible antigenic alterations that coincide with the acid activation of influenza virus A/PR/834-mediated hemolysis. J. Virol. 1983, 48(1):239-248.
38. Yoshimura A., Kuroda K., Kawasaki K., Yamashina S., Maeda T., Ohnishi S. Infectious cell entry mechanism of influenza virus. J. Virol. 1982, 43(1):284-293.