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Review

Virus-like particles as universal influenza vaccines

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Pages 995-1007 | Published online: 09 Jan 2014

References

  • Viboud C, Miller M, Olson D, Osterholm M, Simonsen L. Preliminary estimates of mortality and years of life lost associated with the 2009 A/H1N1 Pandemic in the US and comparison with past influenza seasons. PLoS Curr. RRN1153 (2010).
  • Osterholm MT. Preparing for the next pandemic. N. Engl. J. Med. 352(18), 1839–1842 (2005).
  • Palese P, Compans RW. Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA): mechanism of action. J. Gen. Virol. 33(1), 159–163 (1976).
  • Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J. Virol. 78(22), 12665–12667 (2004).
  • Belshe RB. Current status of live attenuated influenza virus vaccine in the US. Virus Res. 103(1–2), 177–185 (2004).
  • Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM. Predicting the evolution of human influenza A. Science 286(5446), 1921–1925 (1999).
  • Plotkin JB, Dushoff J. Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc. Natl Acad. Sci. USA 100(12), 7152–7157 (2003).
  • Ekiert DC, Bhabha G, Elsliger MA et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324(5924), 246–251 (2009).
  • Buonaguro L, Tornesello ML, Tagliamonte M et al. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol. 80(18), 9134–9143 (2006).
  • Morón G, Rueda P, Casal I, Leclerc C. CD8a-CD11b+ dendritic cells present exogenous virus-like particles to CD8+ T cells and subsequently express CD8a and CD205 molecules. J. Exp. Med. 195(10), 1233–1245 (2002).
  • Aricò E, Wang E, Tornesello ML et al. Immature monocyte derived dendritic cells gene expression profile in response to virus-like particles stimulation. J. Transl. Med. 3, 45 (2005).
  • Morón VG, Rueda P, Sedlik C, Leclerc C. In vivo, dendritic cells can cross-present virus-like particles using an endosome-to-cytosol pathway. J. Immunol. 171(5), 2242–2250 (2003).
  • Song H, Wittman V, Byers A et al. In vitro stimulation of human influenza-specific CD8+ T cells by dendritic cells pulsed with an influenza virus-like particle (VLP) vaccine. Vaccine 28(34), 5524–5532 (2010).
  • Sailaja G, Skountzou I, Quan FS, Compans RW, Kang SM. Human immunodeficiency virus-like particles activate multiple types of immune cells. Virology 362(2), 331–341 (2007).
  • Roy P, Noad R. Virus-like particles as a vaccine delivery system: myths and facts. Hum. Vaccin. 4(1), 5–12 (2008).
  • Johansson BE, Moran TM, Kilbourne ED. Antigen-presenting B cells and helper T cells cooperatively mediate intravirionic antigenic competition between influenza A virus surface glycoproteins. Proc. Natl Acad. Sci. USA 84(19), 6869–6873 (1987).
  • Johansson BE, Kilbourne ED. Dissociation of influenza virus hemagglutinin and neuraminidase eliminates their intravirionic antigenic competition. J. Virol. 67(10), 5721–5723 (1993).
  • Skountzou I, Quan FS, Gangadhara S et al. Incorporation of glycosylphosphatidylinositol-anchored granulocyte-macrophage colony-stimulating factor or CD40 ligand enhances immunogenicity of chimeric simian immunodeficiency virus-like particles. J. Virol. 81(3), 1083–1094 (2007).
  • Wang BZ, Liu W, Kang SM et al. Incorporation of high levels of chimeric human immunodeficiency virus envelope glycoproteins into virus-like particles. J. Virol. 81(20), 10869–10878 (2007).
  • Wang BZ, Quan FS, Kang SM, Bozja J, Skountzou I, Compans RW. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J. Virol. 82(23), 11813–11823 (2008).
  • Vassilieva EV, Wang BZ, Vzorov AN et al. Enhanced mucosal immune responses to HIV virus-like particles containing a membrane-anchored adjuvant. MBio 2(1), e00328–e00310 (2011).
  • Wilson IA, Skehel JJ, Wiley DC. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289(5796), 366–373 (1981).
  • Laver WG, Gerhard W, Webster RG, Frankel ME, Air GM. 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. USA 76(3), 1425–1429 (1979).
  • Laver WG, Air GM, Dopheide TA, Ward CW. Amino acid sequence changes in the haemagglutinin of A/Hong Kong (H3N2) influenza virus during the period 1968–77. Nature 283(5746), 454–457 (1980).
  • Gerhard W, Yewdell J, Frankel ME, Webster R. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290(5808), 713–717 (1981).
  • Wiley DC, Skehel JJ. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56, 365–394 (1987).
  • Krystal M, Elliott RM, Benz EW Jr, Young JF, Palese P. Evolution of influenza A and B viruses: conservation of structural features in the hemagglutinin genes. Proc. Natl Acad. Sci. USA 79(15), 4800–4804 (1982).
  • Wang TT, Tan GS, Hai R et al. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc. Natl Acad. Sci. USA 107(44), 18979–18984 (2010).
  • 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 95(3), 409–417 (1998).
  • Webster RG, Brown LE, Jackson DC. Changes in the antigenicity of the hemagglutinin molecule of H3 influenza virus at acidic pH. Virology 126(2), 587–599 (1983).
  • Vanlandschoot P, Beirnaert E, Barrère B et al. 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. 79 (Pt 7), 1781–1791 (1998).
  • 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. 101(1–2), 13–24 (1988).
  • Wang TT, Tan GS, Hai R et al. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog. 6(2), e1000796 (2010).
  • Sui J, Hwang WC, Perez S et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16(3), 265–273 (2009).
  • Prabhu N, Prabakaran M, Ho HT et al. Monoclonal antibodies against the fusion peptide of hemagglutinin protect mice from lethal influenza A virus H5N1 infection. J. Virol. 83(6), 2553–2562 (2009).
  • Hashem AM, Van Domselaar G, Li C et al. Universal antibodies against the highly conserved influenza fusion peptide cross-neutralize several subtypes of influenza A virus. Biochem. Biophys. Res. Commun. 403(2), 247–251 (2010).
  • Li C, Jaentschke B, Song Y et al. A simple slot blot for the detection of virtually all subtypes of the influenza A viral hemagglutinins using universal antibodies targeting the fusion peptide. Nat. Protoc. 5(1), 14–19 (2010).
  • Horváth A, Tóth GK, Gogolák P et al. A hemagglutinin-based multipeptide construct elicits enhanced protective immune response in mice against influenza A virus infection. Immunol. Lett. 60(2–3), 127–136 (1998).
  • Bianchi E, Liang X, Ingallinella P et al. Universal influenza B vaccine based on the maturational cleavage site of the hemagglutinin precursor. J. Virol. 79(12), 7380–7388 (2005).
  • Bommakanti G, Citron MP, Hepler RW et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc. Natl Acad. Sci. USA 107(31), 13701–13706 (2010).
  • Staneková Z, Király J, Stropkovská A et al. Heterosubtypic protective immunity against influenza A virus induced by fusion peptide of the hemagglutinin in comparison to ectodomain of M2 protein. Acta Virol. 55(1), 61–67 (2011).
  • Steel J, Lowen AC, Wang TT et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 1(1), pii: e00018-10 (2010).
  • Graves PN, Schulman JL, Young JF, Palese P. Preparation of influenza virus subviral particles lacking the HA1 subunit of hemagglutinin: unmasking of cross-reactive HA2 determinants. Virology 126(1), 106–116 (1983).
  • Quan FS, Li ZN, Kim MC et al. Immunogenicity of low-pH treated whole viral influenza vaccine. Virology 417(1), 196–202 (2011).
  • Lamb RA, Lai CJ, Choppin PW. Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc. Natl Acad. Sci. USA 78(7), 4170–4174 (1981).
  • Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell 69(3), 517–528 (1992).
  • Chizhmakov IV, Geraghty FM, Ogden DC, Hayhurst A, Antoniou M, Hay AJ. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. (Lond.) 494 (Pt 2), 329–336 (1996).
  • Mould JA, Drury JE, Frings SM et al. Permeation and activation of the M2 ion channel of influenza A virus. J. Biol. Chem. 275(40), 31038–31050 (2000).
  • Leonov H, Astrahan P, Krugliak M, Arkin IT. How do aminoadamantanes block the influenza M2 channel, and how does resistance develop? J. Am. Chem. Soc. 133(25), 9903–9911 (2011).
  • Lin TI, Heider H, Schroeder C. Different modes of inhibition by adamantane amine derivatives and natural polyamines of the functionally reconstituted influenza virus M2 proton channel protein. J. Gen. Virol. 78 (Pt 4), 767–774 (1997).
  • Iwatsuki-Horimoto K, Horimoto T, Noda T et al. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J. Virol. 80(11), 5233–5240 (2006).
  • McCown MF, Pekosz A. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J. Virol. 79(6), 3595–3605 (2005).
  • Roberts PC, Lamb RA, Compans RW. The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240(1), 127–137 (1998).
  • Roberts PC, Hughey PG, Holsinger LJ, Lamb RA, Compans RW. Effect of influenza A virus M2 protein on virus assembly and release. In: Options for the Control of Influenza III. Brown LE, Hampson AW, Webster RG (Eds). Elsevier, Cairns, Australia, 351–356 (1996).
  • Hughey PG, Roberts PC, Holsinger LJ, Zebedee SL, Lamb RA, Compans RW. Effects of antibody to the influenza A virus M2 protein on M2 surface expression and virus assembly. Virology 212(2), 411–421 (1995).
  • Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451(7178), 591–595 (2008).
  • Stouffer AL, Acharya R, Salom D et al. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451(7178), 596–599 (2008).
  • Hughey PG, Compans RW, Zebedee SL, Lamb RA. Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J. Virol. 66(9), 5542–5552 (1992).
  • Lamb RA, Zebedee SL, Richardson CD. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40(3), 627–633 (1985).
  • Zebedee SL, Lamb RA. Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol. 62(8), 2762–2772 (1988).
  • Fiers W, De Filette M, Birkett A, Neirynck S, Min Jou W. A ‘universal’ human influenza A vaccine. Virus Res. 103(1–2), 173–176 (2004).
  • Liu W, Zou P, Ding J, Lu Y, Chen YH. Sequence comparison between the extracellular domain of M2 protein human and avian influenza A virus provides new information for bivalent influenza vaccine design. Microbes Infect. 7(2), 171–177 (2005).
  • Black RA, Rota PA, Gorodkova N, Klenk HD, Kendal AP. Antibody response to the M2 protein of influenza A virus expressed in insect cells. J. Gen. Virol. 74 (Pt 1) 143–146 (1993).
  • Jegerlehner A, Schmitz N, Storni T, Bachmann MF. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 172(9), 5598–5605 (2004).
  • Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH. The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4(11), 3021–3024 (1985).
  • Treanor JJ, Tierney EL, Zebedee SL, Lamb RA, Murphy BR. Passively transferred monoclonal antibody to the M2 protein inhibits influenza A virus replication in mice. J. Virol. 64(3), 1375–1377 (1990).
  • Slepushkin VA, Katz JM, Black RA, Gamble WC, Rota PA, Cox NJ. Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 13(15), 1399–1402 (1995).
  • Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med. 5(10), 1157–1163 (1999).
  • Fan J, Liang X, Horton MS et al. Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22(23–24), 2993–3003 (2004).
  • De Filette M, Fiers W, Martens W et al. Improved design and intranasal delivery of an M2e-based human influenza A vaccine. Vaccine 24(44–46), 6597–6601 (2006).
  • Ionescu RM, Przysiecki CT, Liang X et al. Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. J. Pharm. Sci. 95(1), 70–79 (2006).
  • Bessa J, Schmitz N, Hinton HJ, Schwarz K, Jegerlehner A, Bachmann MF. Efficient induction of mucosal and systemic immune responses by virus-like particles administered intranasally: implications for vaccine design. Eur. J. Immunol. 38(1), 114–126 (2008).
  • Tompkins SM, Zhao ZS, Lo CY et al. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerging Infect. Dis. 13(3), 426–435 (2007).
  • Fu TM, Grimm KM, Citron MP et al. Comparative immunogenicity evaluations of influenza A virus M2 peptide as recombinant virus like particle or conjugate vaccines in mice and monkeys. Vaccine 27(9), 1440–1447 (2009).
  • Ernst WA, Kim HJ, Tumpey TM et al. Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine 24(24), 5158–5168 (2006).
  • Huleatt JW, Nakaar V, Desai P et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 26(2), 201–214 (2008).
  • De Filette M, Min Jou W, Birkett A et al. Universal influenza A vaccine: optimization of M2-based constructs. Virology 337(1), 149–161 (2005).
  • Heinen PP, Rijsewijk FA, de Boer-Luijtze EA, Bianchi AT. Vaccination of pigs with a DNA construct expressing an influenza virus M2-nucleoprotein fusion protein exacerbates disease after challenge with influenza A virus. J. Gen. Virol. 83(Pt 8), 1851–1859 (2002).
  • Bachmann MF, Rohrer UH, Kündig TM, Bürki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 262(5138), 1448–1451 (1993).
  • De Filette M, Martens W, Roose K et al. An influenza A vaccine based on tetrameric ectodomain of matrix protein 2. J. Biol. Chem. 283(17), 11382–11387 (2008).
  • Song JM, Wang BZ, Park KM et al. Influenza virus-like particles containing M2 induce broadly cross protective immunity. PLoS ONE 6(1), e14538 (2011).
  • Song JM, Van Rooijen N, Bozja J, Compans RW, Kang SM. Vaccination inducing broad and improved cross protection against multiple subtypes of influenza A virus. Proc. Natl Acad. Sci. USA 108(2), 757–761 (2011).
  • Wu F, Yuan XY, Huang WS, Chen YH. Heterosubtypic protection conferred by combined vaccination with M2e peptide and split influenza vaccine. Vaccine 27(43), 6095–6101 (2009).
  • El Bakkouri K, Descamps F, De Filette M et al. Universal vaccine based on ectodomain of matrix protein 2 of influenza A: Fc receptors and alveolar macrophages mediate protection. J. Immunol. 186(2), 1022–1031 (2011).
  • Pei S, Xiong N, Zhang Y, Chen S. Increasing M2 epitope density enhances systemic and mucosal immune responses to influenza A virus. Biotechnol. Lett. 31(12), 1851–1856 (2009).
  • Wei G, Meng W, Guo H et al. Potent neutralization of influenza A virus by a single-domain antibody blocking M2 ion channel protein. PLoS ONE 6(12), e28309 (2011).
  • Turley CB, Rupp RE, Johnson C et al. Safety and immunogenicity of a recombinant M2e-flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine 29(32), 5145–5152 (2011).
  • Taylor DN, Treanor JJ, Strout C et al. Induction of a potent immune response in the elderly using the TLR-5 agonist, flagellin, with a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125, STF2.HA1 SI). Vaccine 29(31), 4897–4902 (2011).
  • Johansson BE, Brett IC. Changing perspective on immunization against influenza. Vaccine 25(16), 3062–3065 (2007).
  • Kilbourne ED, Cerini CP, Khan MW, Mitchell JW Jr, Ogra PL. Immunologic response to the influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. I. Studies in human vaccinees. J. Immunol. 138(9), 3010–3013 (1987).
  • Brett IC, Johansson BE. Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. Virology 339(2), 273–280 (2005).
  • Kilbourne ED, Johansson BE, Grajower B. Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. Proc. Natl Acad. Sci. USA 87(2), 786–790 (1990).
  • Sandbulte MR, Westgeest KB, Gao J et al. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proc. Natl Acad. Sci. USA 108(51), 20748–20753 (2011).
  • Johansson BE, Matthews JT, Kilbourne ED. Supplementation of conventional influenza A vaccine with purified viral neuraminidase results in a balanced and broadened immune response. Vaccine 16(9–10), 1009–1015 (1998).
  • Martinet W, Saelens X, Deroo T et al. Protection of mice against a lethal influenza challenge by immunization with yeast-derived recombinant influenza neuraminidase. Eur. J. Biochem. 247(1), 332–338 (1997).
  • Deroo T, Jou WM, Fiers W. Recombinant neuraminidase vaccine protects against lethal influenza. Vaccine 14(6), 561–569 (1996).
  • Johansson BE. Immunization with influenza A virus hemagglutinin and neuraminidase produced in recombinant baculovirus results in a balanced and broadened immune response superior to conventional vaccine. Vaccine 17(15–16), 2073–2080 (1999).
  • Chen J, Fang F, Li X, Chang H, Chen Z. Protection against influenza virus infection in BALB/c mice immunized with a single dose of neuraminidase-expressing DNAs by electroporation. Vaccine 23(34), 4322–4328 (2005).
  • Chen Z, Kadowaki S, Hagiwara Y et al. Cross-protection against a lethal influenza virus infection by DNA vaccine to neuraminidase. Vaccine 18(28), 3214–3222 (2000).
  • Li X, Fang F, Song Y et al. Essential sequence of influenza neuraminidase DNA to provide protection against lethal viral infection. DNA Cell Biol. 25(4), 197–205 (2006).
  • Qiu M, Fang F, Chen Y et al. Protection against avian influenza H9N2 virus challenge by immunization with hemagglutinin- or neuraminidase-expressing DNA in BALB/c mice. Biochem. Biophys. Res. Commun. 343(4), 1124–1131 (2006).
  • Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, Webby RJ. Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med. 4(2), e59 (2007).
  • Webster RG, Reay PA, Laver WG. Protection against lethal influenza with neuraminidase. Virology 164(1), 230–237 (1988).
  • Sylte MJ, Hubby B, Suarez DL. Influenza neuraminidase antibodies provide partial protection for chickens against high pathogenic avian influenza infection. Vaccine 25(19), 3763–3772 (2007).
  • 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. 80(4), 1959–1964 (2006).
  • Qiao CL, Yu KZ, Jiang YP et al. Protection of chickens against highly lethal H5N1 and H7N1 avian influenza viruses with a recombinant fowlpox virus co-expressing H5 haemagglutinin and N1 neuraminidase genes. Avian Pathol. 32(1), 25–32 (2003).
  • Pavlova SP, Veits J, Keil GM, Mettenleiter TC, Fuchs W. Protection of chickens against H5N1 highly pathogenic avian influenza virus infection by live vaccination with infectious laryngotracheitis virus recombinants expressing H5 hemagglutinin and N1 neuraminidase. Vaccine 27(5), 773–785 (2009).
  • Bright RA, Carter DM, Crevar CJ et al. Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle. PLoS ONE 3(1), e1501 (2008).
  • Pushko P, Tumpey TM, Van Hoeven N et al. Evaluation of influenza virus-like particles and Novasome adjuvant as candidate vaccine for avian influenza. Vaccine 25(21), 4283–4290 (2007).
  • Bright RA, Carter DM, Daniluk S et al. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 25(19), 3871–3878 (2007).
  • Quan FS, Kim MC, Lee BJ, Song JM, Compans RW, Kang SM. Influenza M1 VLPs containing neuraminidase induce heterosubtypic cross-protection. Virology 430(2), 127–135 (2012).
  • Compans RW, Dimmock NJ, Meier-Ewert H. Effect of antibody to neuraminidase on the maturation and hemagglutinating activity of an influenza A2 virus. J. Virol. 4(4), 528–534 (1969).
  • Schulman JL, Khakpour M, Kilbourne ED. Protective effects of specific immunity to viral neuraminidase on influenza virus infection of mice. J. Virol. 2(8), 778–786 (1968).
  • Webster RG, Laver WG, Kilbourne ED. Reactions of antibodies with surface antigens of influenza virus. J. Gen. Virol. 3(3), 315–326 (1968).
  • Kasel JA, Couch RB, Gerin JL, Schulman JL. Effect of influenza anti-neuraminidase antibody on virus neutralization. Infect. Immun. 8(1), 130–131 (1973).
  • Johansson BE, Kilbourne ED. Immunization with dissociated neuraminidase, matrix, and nucleoproteins from influenza A virus eliminates cognate help and antigenic competition. Virology 225(1), 136–144 (1996).
  • Johansson BE, Bucher DJ, Kilbourne ED. Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J. Virol. 63(3), 1239–1246 (1989).
  • Song JM, Hossain J, Yoo DG et al. Protective immunity against H5N1 influenza virus by a single dose vaccination with virus-like particles. Virology 405(1), 165–175 (2010).
  • Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med. 11(Suppl. 4), S63–S68 (2005).
  • Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 124(4), 783–801 (2006).
  • Kang SM, Compans RW. Host responses from innate to adaptive immunity after vaccination: molecular and cellular events. Mol. Cells 27(1), 5–14 (2009).
  • Kool M, Pétrilli V, De Smedt T et al. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol. 181(6), 3755–3759 (2008).
  • Sato A, Iwasaki A. Induction of antiviral immunity requires Toll-like receptor signaling in both stromal and dendritic cell compartments. Proc. Natl Acad. Sci. USA 101(46), 16274–16279 (2004).
  • Lambrecht BN, Prins JB, Hoogsteden HC. Lung dendritic cells and host immunity to infection. Eur. Respir. J. 18(4), 692–704 (2001).
  • Kwissa M, Kasturi SP, Pulendran B. The science of adjuvants. Expert Rev. Vaccines 6(5), 673–684 (2007).
  • Pulendran B, Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 124(4), 849–863 (2006).
  • Zinkernagel RM. Immunology taught by viruses. Science 271(5246), 173–178 (1996).
  • Bachmann MF, Zinkernagel RM, Oxenius A. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 161(11), 5791–5794 (1998).
  • Quan FS, Huang C, Compans RW, Kang SM. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol. 81(7), 3514–3524 (2007).
  • McBurney SP, Young KR, Ross TM. Membrane embedded HIV-1 envelope on the surface of a virus-like particle elicits broader immune responses than soluble envelopes. Virology 358(2), 334–346 (2007).
  • Kang SM, Yoo DG, Lipatov AS et al. Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS ONE 4(3), e4667 (2009).
  • Bachmann MF, Lutz MB, Layton GT et al. Dendritic cells process exogenous viral proteins and virus-like particles for class I presentation to CD8+ cytotoxic T lymphocytes. Eur. J. Immunol. 26(11), 2595–2600 (1996).
  • Storni T, Lechner F, Erdmann I et al. Critical role for activation of antigen-presenting cells in priming of cytotoxic T cell responses after vaccination with virus-like particles. J. Immunol. 168(6), 2880–2886 (2002).
  • Storni T, Ruedl C, Schwarz K, Schwendener RA, Renner WA, Bachmann MF. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J. Immunol. 172(3), 1777–1785 (2004).
  • Guo L, Lu X, Kang SM, Chen C, Compans RW, Yao Q. Enhancement of mucosal immune responses by chimeric influenza HA/SHIV virus-like particles. Virology 313(2), 502–513 (2003).
  • Yao Q, Zhang R, Guo L, Li M, Chen C. Th cell-independent immune responses to chimeric hemagglutinin/simian human immunodeficiency virus-like particles vaccine. J. Immunol. 173(3), 1951–1958 (2004).
  • Zhang R, Zhang S, Li M, Chen C, Yao Q. Incorporation of CD40 ligand into SHIV virus-like particles (VLP) enhances SHIV-VLP-induced dendritic cell activation and boosts immune responses against HIV. Vaccine 28(31), 5114–5127 (2010).
  • Pandey JP. Comment on Flagellin as an adjuvant: cellular mechanisms and potential. J. Immunol. 186(3), 1299; author reply 1299 (2011).
  • Mizel SB, Bates JT. Flagellin as an adjuvant: cellular mechanisms and potential. J. Immunol. 185(10), 5677–5682 (2010).
  • Quan FS, Compans RW, Nguyen HH, Kang SM. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol. 82(3), 1350–1359 (2008).
  • Wang BZ, Xu R, Quan FS, Kang SM, Wang L, Compans RW. Intranasal immunization with influenza VLPs incorporating membrane-anchored flagellin induces strong heterosubtypic protection. PLoS ONE 5(11), e13972 (2010).
  • Wei HJ, Chang W, Lin SC et al. Fabrication of influenza virus-like particles using M2 fusion proteins for imaging single viruses and designing vaccines. Vaccine 29(41), 7163–7172 (2011).
  • Smith LR, Wloch MK, Ye M et al. Phase 1 clinical trials of the safety and immunogenicity of adjuvanted plasmid DNA vaccines encoding influenza A virus H5 hemagglutinin. Vaccine 28(13), 2565–2572 (2010).
  • Lalor PA, Webby RJ, Morrow J et al. Plasmid DNA-based vaccines protect mice and ferrets against lethal challenge with A/Vietnam/1203/04 (H5N1) influenza virus. J. Infect. Dis. 197(12), 1643–1652 (2008).
  • Price GE, Soboleski MR, Lo CY et al. Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 influenza A viruses. Vaccine 27(47), 6512–6521 (2009).
  • Jimenez GS, Planchon R, Wei Q et al. Vaxfectin-formulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum. Vaccin. 3(5), 157–164 (2007).
  • Nayak DP, Balogun RA, Yamada H, Zhou ZH, Barman S. Influenza virus morphogenesis and budding. Virus Res. 143(2), 147–161 (2009).

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