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Review

Proteosome-adjuvanted intranasal influenza vaccines: advantages, progress and future considerations

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Pages 365-375 | Published online: 09 Jan 2014

References

  • Fiore AE, Shay DK, Broder K et al.; Centers for Disease Control and Prevention. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR58, 1–52 (2009).
  • Centers for Disease Control and Prevention (CDC). Influenza vaccination coverage among children and adults – United States, 2008–09 influenza season. MMWR58, 1091–1095 (2009).
  • Gasparini R, Laghi-Pasini F, Staniscia T et al. A. MF59-adjuvanted H5N1 vaccine induces immunologic memory and heterotypic antibody responses in non-elderly and elderly adults. PLoS One4(2), e4384 (2009).
  • Walker WT, Oeser C, Reiner A et al. Safety and immunogenicity of AS03B adjuvanted split virion versus non-adjuvanted whole virion H1N1 influenza vaccine in UK children aged 6 months-12 years: open label, randomised, parallel group, multicentre study. Br. Med. J.340, c2649 (2010).
  • Baras B, Bouveret N, Devaster JM et al. A vaccine manufacturer’s approach to address medical needs related to seasonal and pandemic influenza viruses. Influenza Other Respi. Viruses2(6), 251–260 (2008).
  • Nir Y, Paz A, Sabo E, Potasman I. Fear of injections in young adults: prevalence and associations. Am. J. Trop. Med. Hyg.68(3), 341–344 (2003).
  • Breau L, McGrath PJ, Craig K, Santor D, Cassidy KL, Reid G. Facial expression of children receiving immunizations: a principal components analysis of the child facial coding system. Clin. J. Pain17(2), 178–186 (2001).
  • Sendi P, Locher R, Bucheli B et al. Intranasal influenza vaccine in a working population. Clin. Infect. Dis.38(7), 974–980 (2004).
  • Glenn GM, Thomas DN, Poffenberger KL et al. Safety and immunogenicity of an influenza vaccine A/H5N1 (A/Vietnam/1194/2004) when coadministered with a heat-labile enterotoxin (LT) adjuvant patch. Vaccine27(Suppl. 6), 60–66 (2009).
  • Tamura S. Studies on the usefulness of intranasal inactivated influenza vaccines. Vaccine28(38), 6393–6397 (2010).
  • Song JH, Nguyen HH, Cuburu N et al. Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc. Natl Acad. Sci. USA105(5), 1644–1649 (2008).
  • Prabakaran M, Madhan S, Prabhu N, Geng GY, New R, Kwang J. Reverse micelle-encapsulated recombinant baculovirus as an oral vaccine against H5N1 infection in mice. Antiviral Res.86(2), 180–187 (2010).
  • Ambrose CS, Luke C, Coelingh K. Current status of live attenuated influenza vaccine in the United States for seasonal and pandemic influenza. Influenza Other Respi. Viruses2(6), 193–202 (2008).
  • Waldman RH, Bond JO, Levitt LP et al. An evaluation of influenza immunization. influence of route of administration and vaccine strain. Bull. World Health Organ.41(3), 543–548 (1969).
  • Liem KS, Jacobs J, Marcus EA, van Strik R. The protective effect of intranasal immunization with inactivated influenza virus vaccine. Postgrad. Med. J.49(569), 175–179 (1973).
  • Lycke N, Holmgren J. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology59(2), 301–308 (1986).
  • Sixma TK, Kalk KH, van Zanten BA et al. Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J. Mol. Biol.230(3), 890–918 (1993).
  • Glück U, Gebbers JO, Glück R. Phase 1 evaluation of intranasal virosomal influenza vaccine with and without Escherichia coli heat-labile toxin in adult volunteers. J. Virol.73(9), 7780–7786 (1999).
  • Mutsch M, Zhou W, Rhodes P et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell’s palsy in Switzerland. N. Engl. J. Med.350(9), 896–903 (2004).
  • van Ginkel FW, Jackson RJ, Yuki Y, McGhee JR. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J. Immunol.165(9), 4778–4782 (2000).
  • Baldridge JR, Yorgensen Y, Ward JR, Ulrich JT. Monophosphoryl lipid A enhances mucosal and systemic immunity to vaccine antigens following intranasal administration. Vaccine18(22), 2416–2425 (2000).
  • Xiaowen Z, Qinghua Y, Xiaofei Z, Qian Y. Co-administration of inactivated avian influenza virus with CpG or rIL-2 strongly enhances the local immune response after intranasal immunization in chicken. Vaccine27(41), 5628–5632 (2009).
  • Hu KF, Lövgren-Bengtsson K, Morein B. Immunostimulating complexes (ISCOMs) for nasal vaccination. Adv. Drug Deliv. Rev.51(1–3), 149–159 (2001).
  • Boyce TG, Hsu HH, Sannella EC et al. Safety and immunogenicity of adjuvanted and unadjuvanted subunit influenza vaccines administered intranasally to healthy adults. Vaccine19(2–3), 217–226 (2000).
  • Ichinohe T, Watanabe I, Ito S et al. Synthetic double-stranded RNA poly(I:C) combined with mucosal vaccine protects against influenza virus infection. J. Virol.79(5), 2910–2919 (2005).
  • Jabbal-Gill I, Fisher A, Illum L et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine23(35), 4367–4374 (2005).
  • Kiyono H, Fukuyama S. NALT-versus Peyer’s-patch-mediated mucosal immunity. Nat. Rev. Immunol.4(9), 699–710 (2004).
  • Renegar KB, Small PA Jr, Boykins LG, Wright PF. Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J. Immunol.173(3), 1978–1986 (2004).
  • Mazanec MB, Lamm ME, Lyn D, Portner A, Nedrud JG. Comparison of IgA versus IgG monoclonal antibodies for passive immunization of the murine respiratory tract. Virus Res.23(1–2), 1–12 (1992).
  • Renegar KB, Jackson GD, Mestecky J. In vitro comparison of the biologic activities of monoclonal monomeric IgA, polymeric IgA, and secretory IgA. J. Immunol.160(3), 1219–1223 (1998).
  • Liew FY, Russell SM, Appleyard G, Brand CM, Beale J. Cross-protection in mice infected with influenza A virus by the respiratory route is correlated with local IgA antibody rather than serum antibody or cytotoxic T cell reactivity. Eur. J. Immunol.14(4), 350–356 (1984).
  • Tamura SI, Asanuma H, Ito Y et al. Superior cross-protective effect of nasal vaccination to subcutaneous inoculation with influenza hemagglutinin vaccine. Eur. J. Immunol.22(2), 477–481 (1992).
  • Ichinohe T, Kawaguchi A, Tamura SI et al. Intranasal immunization with H5N1 vaccine plus poly I:poly C12U, a Toll-like receptor agonist, protects mice against homologous and heterologous virus challenge. Microbes Infect.9(11), 1333–1340 (2007).
  • Tumpey TM, Renshaw M, Clements JD, Katz JM. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J. Virol.75(11), 5141–5150 (2001).
  • Mendelman PM, Rappaport R, Cho I et al. Live attenuated influenza vaccine induces cross-reactive antibody responses in children against an a/Fujian/411/2002-like H3N2 antigenic variant strain. Pediatr. Infect. Dis. J.23(11), 1053–1055 (2004).
  • Belshe RB, Gruber WC, Mendelman PM et al. Efficacy of vaccination with live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine against a variant (A/Sydney) not contained in the vaccine. J. Pediatr.136(2), 168–175 (2000).
  • Asahi Y, Yoshikawa T, Watanabe I et al. Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines. J. Immunol.168(6), 2930–2938 (2002).
  • Taylor HP, Dimmock NJ. Mechanism of neutralization of influenza virus by secretory IgA is different from that of monomeric IgA or IgG. J. Exp. Med.161(1), 198–209 (1985).
  • Lowell GH, Smith LF, Seid RC, Zollinger WD. Peptides bound to proteosomes via hydrophobic feet become highly immunogenic without adjuvants. J. Exp. Med.167(2), 658–663 (1988).
  • Wetzler LM. Immunopotentiating ability of neisserial major outer membrane proteins. Use as an adjuvant for poorly immunogenic substances and potential use in vaccines. Ann. NY Acad. Sci.15(730), 367–370 (1994).
  • VanCott TC, Kaminski RW, Mascola JR et al. HIV-1 neutralizing antibodies in the genital and respiratory tracts of mice intranasally immunized with oligomeric gp160. J. Immunol.160(4), 2000–2012 (1998).
  • Cyr SL, Jones T, Stoica-Popescu I et al. Intranasal proteosome™-based respiratory syncytial virus (RSV) vaccines protect BALB/c mice against challenge without eosinophilia or enhanced pathology. Vaccine25(29), 5378–5389 (2007).
  • Batzloff MR, Yan H, Davies MR et al. Toward the development of an antidisease, transmission-blocking intranasal vaccine for group a streptococcus. J. Infect. Dis.192(8), 1450–1455 (2005).
  • Mallett CP, Hale TL, Kaminski RW et al. Intransal or intragastric immunization with proteosome-Shigella lipopolysaccharide vaccines protects against lethal pneumonia in a murine model of Shigella infection. Infect. Immun.63(6), 2382–2386 (1995).
  • Jones T, Cyr S, Allard F, Bellerose N, Lowell GH, Burt DS. Protollin™: a novel adjuvant for intranasal vaccines. Vaccine22(27–28), 3691–3697 (2004).
  • Langley JM, Halperin SA, McNeil S et al. Safety and immunogenicity of a Proteosome™-trivalent inactivated influenza vaccine, given nasally to healthy adults. Vaccine24(10), 1601–1608 (2006).
  • Pasetti MF, Resendiz-Albor A, Ramirez K et al. Heterologous prime-boost strategy to immunize very young infants against measles: pre-clinical studies in rhesus macaques. Clin. Pharmacol. Ther.82(6), 672–685 (2007).
  • Hu MC, Jones T, Kenney RT, Barnard DL, Burt DS, Lowell GH. Intranasal Protollin-formulated recombinant SARS S-protein elicits respiratory and serum neutralizing antibodies and protection in mice. Vaccine25(34), 6334–6340 (2007).
  • Lynch EC, Blake MS, Gotschlich EC, Mauro A. Studies of porins: spontaneously transferred from whole cells and reconstituted from purified proteins of Neisseria gonorrhoeae and Neisseria meningitidis. Biophys. J.45(1), 104–107 (1984).
  • Massari P, Henneke P, Ho Y, Latz E, Golenbock DT, Wetzler LM. Cutting edge: immune stimulation by neisserial porins is Toll-like receptor 2 and MyD88 dependent. J. Immunol.168(4), 1533–1537 (2002).
  • Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem.274(16), 10689–10692 (1999).
  • Faure E, Thomas L, Xu H, Medvedev A, Equils O, Arditi M. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kappa B activation. J. Immunol.166(3), 2018–2024 (2001).
  • Chabot SM, Chernin TS, Shawi M et al. TLR-2 activation by proteosomes promotes uptake of particulate vaccines at mucosal surfaces. Vaccine25(29), 5348–5358 (2007).
  • Levi R, Aboud-Pirak E, Leclerc C, Lowell GH, Arnon R. Intranasal immunization of mice against influenza with synthetic peptides anchored to proteosomes. Vaccine13(14), 1353–1359 (1995).
  • Plante M, Jones T, Allard F et al. Nasal immunization with subunit proteosome influenza vaccines induces serum HAI, mucosal IgA and protection against influenza challenge. Vaccine20(1–2), 218–225 (2001).
  • Jones T, Allard F, Cyr SL et al. A nasal Proteosome™ influenza vaccine containing baculovirus-derived hemagglutinin induces protective mucosal and systemic immunity. Vaccine21(25–26), 3706–3712 (2003).
  • Lowell GL, Burt D, White G, Fries L. Proteosome technology for vaccines and adjuvants. In: New Generation Vaccines. Levine M (Ed.). Marcel Decker Inc., NY, USA, 271–282 (2004).
  • Reuman PD, Keely S, Schiff GM. Assessment of signs of influenza illness in the ferret model. J. Virol. Methods24(1–2), 27–34 (1989).
  • Frenkel D, Puckett L, Petrovic S et al. A nasal proteosome adjuvant activates microglia and prevents amyloid deposition. Ann. Neurol.63(5), 591–601 (2008).
  • Treanor J, Nolan C, O’Brien D et al. Intranasal administration of a proteosome–influenza vaccine is well-tolerated and induces serum and nasal secretion influenza antibodies in healthy human subjects. Vaccine24(3), 254–262 (2006).
  • Fries L, Lambkin R, Gelder C et al. FluInsure™, an inactivated trivalent influenza vaccine for intranasal administration, is protective in human challenge with A/Panama/2007/99 (H3N2) virus. Presented at: International Conference on Options for the Control of Influenza V. Okinawa, Japan, 7–11 October 2003.
  • Langley JM, Akoi F, Ward BJ et al. A nasally administered trivalent inactivated influenza vaccine is well tolerated, stimulates both mucosal and systemic immunity, and potentially protects against influenza illness. Vaccine29(10), 1921–1928 (2011).
  • Ambrose CS, Luke C, Coelingh K. Current status of live attenuated influenza vaccine in the United States for seasonal and pandemic influenza. Influenza Other Respi. Viruses.2(6), 193–202 (2008).
  • Herrera GA, Iwane MK, Cortese M et al. Influenza vaccine effectiveness among 50–64-year-old persons during a season of poor antigenic match between vaccine and circulating influenza virus strains: Colorado, United States, 2003–2004. Vaccine25(1), 154–160 (2007).
  • Belshe RB, Mendelman PM, Treanor J et al. The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine in children. N. Engl. J. Med.338(20), 1405–1412 (1998).
  • Jabbal-Gill I. Nasal vaccine innovation. J. Drug Targeting18(10), 771–786 (2010).
  • FluMist™, Influenza Vaccine Live, Intranasal. Prescribing Information. MedImmune, Gaithersburg, MD, USA (2007).
  • Rhorer J, Ambrose CS, Dickinson S et al. Efficacy of live attenuated influenza vaccine in children: a meta-analysis of nine randomized clinical trials. Vaccine27(7), 1101–1110 (2009).
  • Govaert TM, Thijs CT, Masurel N et al. The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA272, 1661–1665 (1997).
  • Ruben FL. Prevention and control of influenza. Role of vaccine. Am. J. Med.82(6A), 31–34 (1987).
  • Johnson PR, Feldman S, Thompson JM, Mahoney JD, Wright PF. Immunity to influenza A virus infection in young children: a comparison of natural infection, live cold-adapted vaccine, and inactivated vaccine. J. Infect. Dis.154(1), 121–127 (1986).
  • McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med.309(1), 13–17 (1983).
  • Forrest BD, Pride MW, Dunning AJ et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin. Vaccine Immunol.15(7), 1042–1053 (2008).
  • Fries LF, Montemarano AD, Mallett CP, Taylor DN, Hale TL, Lowell GH. Safety and immunogenicity of a proteosome-Shigella flexneri 2a lipopolysaccharide vaccine administered intranasally to healthy adults. Infect. Immun.69(7), 4545–4553 (2001).

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