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Review

Influenza virosomes as a vaccine adjuvant and carrier system

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Pages 437-446 | Published online: 09 Jan 2014

References

  • Ribeiro CMS, Schijns VEJC. Immunology of vaccine adjuvants. In: Vaccine Adjuvants. Davies G (Ed.). Springer, Berlin, Germany 1–14 (2010).
  • Wilson-Welder JH, Torres MP, Kipper MJ, Mallapragada SK, Wannemuehler MJ, Narasimhan B. Vaccine adjuvants: current challenges and future approaches. J. Pharm. Sci.98(4), 1278–1316 (2009).
  • Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol.10(11), 787–796 (2010).
  • Ishii KJ, Akira S. Toll or Toll-free adjuvant path toward the optimal vaccine development. J. Clin. Immunol.27(4), 363–371 (2007).
  • Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med.11(Suppl. 4), S63–S68 (2005).
  • De Gregorio E, D’Oro U, Wack A. Immunology of TLR-independent vaccine adjuvants. Curr. Opin. Immunol.21(3), 339–345 (2009).
  • Kool M, Petrilli 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).
  • Tritto E, Mosca F, De Gregorio E. Mechanism of action of licensed vaccine adjuvants. Vaccine27(25–26), 3331–3334 (2009).
  • Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity33(4), 492–503 (2010).
  • Macagno A, Napolitani G, Lanzavecchia A, Sallusto F. Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol.28(5), 227–233 (2007).
  • Harandi AM, Davies G, Olesen OF. Vaccine adjuvants: scientific challenges and strategic initiatives. Expert Rev. Vaccines8(3), 293–298 (2009).
  • Petrovsky N. Freeing vaccine adjuvants from dangerous immunological dogma. Expert Rev. Vaccines7(1), 7–10 (2008).
  • Sesardic D. Regulatory considerations on new adjuvants and delivery systems. Vaccine24(Suppl. 2), S2–S7 (2006).
  • Mastelic B, Ahmed S, Egan WM et al. Mode of action of adjuvants: implications for vaccine safety and design. Biologicals38(5), 594–601 (2010).
  • Pink JR, Kieny MP. 4th meeting on novel adjuvants currently in/close to human clinical testing World Health Organization – organisation Mondiale de la Sante Fondation Merieux, Annecy, France, 23–25 June 2003. Vaccine22(17–18), 2097–2102 (2004).
  • The European Agency for the Evaluation of Medicinal Products. Guideline on adjuvants in vaccines. EMA, London, UK (2004).
  • Grgacic EV, Anderson DA. Virus-like particles: passport to immune recognition. Methods40(1), 60–65 (2006).
  • Jennings GT, Bachmann MF. The coming of age of virus-like particle vaccines. Biol. Chem.389(5), 521–536 (2008).
  • Jansen KU, Conner ME, Estes MK. Virus-like particles as vaccines and vaccine delivery systems. In: New Generation Vaccines. Levine MM, Dougan G, Good MF et al. (Eds). Informa Healthcare, London, UK, 298–305 (2010).
  • Haynes JR. Influenza virus-like particle vaccines. Expert Rev. Vaccines8(4), 435–445 (2009).
  • Cox MM. Progress on baculovirus-derived influenza vaccines. Curr. Opin. Mol. Ther.10(1), 56–61 (2008).
  • Gluck R, Mischler R, Brantschen S, Just M, Althaus B, Cryz SJ Jr. Immunopotentiating reconstituted influenza virus virosome vaccine delivery system for immunization against hepatitis A. J. Clin. Invest.90(6), 2491–2495 (1992).
  • Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr. Opin. Biotechnol.18(6), 537–545 (2007).
  • Smith ML, Fitzmaurice WP, Turpen TH, Palmer KE. Display of peptides on the surface of tobacco mosaic virus particles. Curr. Top. Microbiol. Immunol.332, 13–31 (2009).
  • Buonaguro L, Tornesello ML, Buonaguro FM. Virus-like particles as particulate vaccines. Curr. HIV Res.8(4), 299–309 (2010).
  • 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).
  • Morein B, Helenius A, Simons K, Pettersson R, Kaariainen L, Schirrmacher V. Effective subunit vaccines against an enveloped animal virus. Nature276(5689), 715–718 (1978).
  • Almeida JD, Edwards DC, Brand CM, Heath TD. Formation of virosomes from influenza subunits and liposomes. Lancet2(7941), 899–901 (1975).
  • Stegmann T, Kamphuis T, Meijerhof T, Goud E, de Haan A, Wilschut J. Lipopeptide-adjuvanted respiratory syncytial virus virosomes: a safe and immunogenic non-replicating vaccine formulation. Vaccine28(34), 5543–5550 (2010).
  • Datta SA, Rein A. Preparation of recombinant HIV-1 gag protein and assembly of virus-like particles in vitro. Methods Mol. Biol.485, 197–208 (2009).
  • Stegmann T, Morselt HW, Booy FP, van Breemen JF, Scherphof G, Wilschut J. Functional reconstitution of influenza virus envelopes. EMBO J.6(9), 2651–2659 (1987).
  • Mischler R , Metcalfe IC. Inflexal V a trivalent virosome subunit influenza vaccine: production. Vaccine20(Suppl. 5), B17–B23 (2002).
  • Bovier PA. Epaxal: a virosomal vaccine to prevent hepatitis A infection. Expert Rev. Vaccines7(8), 1141–1150 (2008).
  • Herzog C, Hartmann K, Kunzi V et al. Eleven years of Inflexal V-a virosomal adjuvanted influenza vaccine. Vaccine27(33), 4381–4387 (2009).
  • Wiedermann U, Wiltschke C, Jasinska J et al. A virosomal formulated Her-2/neu multi-peptide vaccine induces Her-2/neu-specific immune responses in patients with metastatic breast cancer: a Phase I study. Breast Cancer Res. Treat.119(3), 673–683 (2010).
  • Genton B, Pluschke G, Degen L et al. A randomized placebo-controlled Phase Ia malaria vaccine trial of two virosome-formulated synthetic peptides in healthy adult volunteers. PLoS ONE2(10), e1018 (2007).
  • Thompson FM, Porter DW, Okitsu SL et al. Evidence of blood stage efficacy with a virosomal malaria vaccine in a Phase IIa clinical trial. PLoS ONE3(1), e1493 (2008).
  • Lamb RA, Krug RM. Orthomyxoviridae: the viruses and their replication. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, Philadelphia, PA, USA, 1487–1531 (2001).
  • Daemen T, de Mare A, Bungener L, de Jonge J, Huckriede A, Wilschut J. Virosomes for antigen and DNA delivery. Adv. Drug Deliv. Rev.57(3), 451–463 (2005).
  • Moser C, Amacker M, Kammer AR, Rasi S, Westerfeld N, Zurbriggen R. Influenza virosomes as a combined vaccine carrier and adjuvant system for prophylactic and therapeutic immunizations. Expert Rev. Vaccines6(5), 711–721 (2007).
  • Felnerova D, Viret JF, Gluck R, Moser C. Liposomes and virosomes as delivery systems for antigens, nucleic acids and drugs. Curr. Opin. Biotechnol.15(6), 518–529 (2004).
  • Khoshnejad M, Young PR, Toth I, Minchin RF. Modified influenza virosomes: recent advances and potential in gene delivery. Curr. Med. Chem.14(29), 3152–3156 (2007).
  • Markgraf K, Muller K, Ponimaskin EG, Rudolph M, Schmidt MF, Herrmann A. Lipid composition of virosomes modulates their fusion efficiency with cryopreserved bull sperm cells. Cloning3(1), 11–21 (2001).
  • Cusi MG, Terrosi C, Savellini GG, Di Genova G, Zurbriggen R, Correale P. Efficient delivery of DNA to dendritic cells mediated by influenza virosomes. Vaccine22(5–6), 735–739 (2004).
  • de Jonge J, Leenhouts JM, Holtrop M et al. Cellular gene transfer mediated by influenza virosomes with encapsulated plasmid DNA. Biochem. J.405(1), 41–49 (2007).
  • Kammer AR, Amacker M, Rasi S et al. A new and versatile virosomal antigen delivery system to induce cellular and humoral immune responses. Vaccine25(41), 7065–7074 (2007).
  • Wilschut J, de Jonge J, Huckriede A, Amorij JP, Hinrichs WL, Frijlink HW. Preservation of influenza virosome structure and function during freeze-drying and storage. J. Liposome Res.17(3–4), 173–182 (2007).
  • Amacker M, Engler O, Kammer AR et al. Peptide-loaded chimeric influenza virosomes for efficient in vivo induction of cytotoxic T cells. Int. Immunol.17(6), 695–704 (2005).
  • Zurbriggen R, Gluck R. Immunogenicity of IRIV- versus alum-adjuvanted diphtheria and tetanus toxoid vaccines in influenza primed mice. Vaccine17(11–12), 1301–1305 (1999).
  • Westerfeld N, Zurbriggen R. Peptides delivered by immunostimulating reconstituted influenza virosomes. J. Pept. Sci.11(11), 707–712 (2005).
  • Okitsu SL, Mueller MS, Amacker M et al. Preclinical profiling of the immunogenicity of a two-component subunit malaria vaccine candidate based on virosome technology. Hum. Vaccin.4(2), 106–114 (2008).
  • Nallet S, Amacker M, Westerfeld N et al. Respiratory syncytial virus subunit vaccine based on a recombinant fusion protein expressed transiently in mammalian cells. Vaccine27(46), 6415–6419 (2009).
  • Liu X, Siegrist S, Amacker M, Zurbriggen R, Pluschke G, Seeberger PH. Enhancement of the immunogenicity of synthetic carbohydrates by conjugation to virosomes: a leishmaniasis vaccine candidate. ACS Chem. Biol.1(3), 161–164 (2006).
  • Zurbriggen R, Amacker M, Kammer AR et al. Virosome-based active immunization targets soluble amyloid species rather than plaques in a transgenic mouse model of Alzheimer’s disease. J. Mol. Neurosci.27(2), 157–166 (2005).
  • Correale P, Del Vecchio MT, Renieri T et al. Anti-angiogenetic effects of immune-reconstituted influenza virosomes assembled with parathyroid hormone-related protein derived peptide vaccine. Cancer Lett.263(2), 291–301 (2008).
  • Kopp N, Diaz D, Amacker M et al. Identification of a synthetic peptide inducing cross-reactive antibodies binding to Rhipicephalus (Boophilus) decoloratus, Rhipicephalus (Boophilus) microplus, Hyalomma anatolicum anatolicum and Rhipicephalus appendiculatus BM86 homologues. Vaccine28(1), 261–269 (2009).
  • Waelti E, Wegmann N, Schwaninger R et al. Targeting Her-2/neu with antirat Neu virosomes for cancer therapy. Cancer Res.62(2), 437–44 (2002).
  • Amacker M, Moese S, Kammer AR, Helenius A, Zurbriggen R. Influenza virosomes as delivery systems for antigens. In: Delivery Technologies for Biopharmaceuticals: Peptides, Proteins, Nucleic Acids, and Vaccines. Jorgensen L, Nielsen HM (Eds). John Wiley & Sons Ltd., Chichester, UK, 377–393 (2009).
  • Huckriede A, Bungener L, Stegmann T et al. The virosome concept for influenza vaccines. Vaccine23(Suppl. 1), S26–S38 (2005).
  • Bungener L, Huckriede A, de Mare A, de Vries-Idema J, Wilschut J, Daemen T. Virosome-mediated delivery of protein antigens in vivo: efficient induction of class I MHC-restricted cytotoxic T lymphocyte activity. Vaccine23(10), 1232–1241 (2005).
  • Schumacher R, Amacker M, Neuhaus D et al. Efficient induction of tumoricidal cytotoxic T lymphocytes by HLA-A0201 restricted, melanoma associated, L(27)Melan-A/MART-1(26–35) peptide encapsulated into virosomes in vitro. Vaccine23(48–49), 5572–5582 (2005).
  • Angel J, Chaperot L, Molens JP et al. Virosome-mediated delivery of tumor antigen to plasmacytoid dendritic cells. Vaccine25(19), 3913–3921 (2007).
  • Bungener L, Serre K, Bijl L et al. Virosome-mediated delivery of protein antigens to dendritic cells. Vaccine20(17–18), 2287–2295 (2002).
  • Noad R, Roy P. Virus-like particles as immunogens. Trends Microbiol.11(9), 438–444 (2003).
  • Hofer U, Lehmann AD, Waelti E, Amacker M, Gehr P, Rothen-Rutishauser B. Virosomes can enter cells by non-phagocytic mechanisms. J. Liposome Res.19(4), 301–309 (2009).
  • Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol.38(5), 1404–1413 (2008).
  • Junt T, Moseman EA, Iannacone M et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature450(7166), 110–114 (2007).
  • Carrasco YR, Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity27(1), 160–171 (2007).
  • Bachmann MF, Speiser DE, Ohashi PS. Functional management of an antiviral cytotoxic T-cell response. J. Virol.71(8), 5764–5768 (1997).
  • Justewicz DM, Doherty PC, Webster RG. The B-cell response in lymphoid tissue of mice immunized with various antigenic forms of the influenza virus hemagglutinin. J. Virol.69(9), 5414–5421 (1995).
  • Liu WC, Lin SC, Yu YL, Chu CL, Wu SC. Dendritic cell activation by recombinant hemagglutinin proteins of H1N1 and H5N1 influenza A viruses. J. Virol.84(22), 12011–12017 (2010).
  • 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. Vaccine28(34), 5524–5532 (2010).
  • Barton GM. Viral recognition by Toll-like receptors. Semin. Immunol.19(1), 33–40 (2007).
  • Schumacher R, Adamina M, Zurbriggen R et al. Influenza virosomes enhance class I restricted CTL induction through CD4+ T cell activation. Vaccine22, 714–723 (2004).
  • McCoy K, Tatsis N, Korioth-Schmitz B et al. Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J. Virol.81(12), 6594–6604 (2007).
  • Sharpe S, Polyanskaya N, Dennis M et al. Induction of simian immunodeficiency virus (SIV)-specific CTL in rhesus macaques by vaccination with modified vaccinia virus Ankara expressing SIV transgenes: influence of pre-existing anti-vector immunity. J. Gen. Virol.82(Pt 9), 2215–2223 (2001).
  • Jegerlehner A, Wiesel M, Dietmeier K et al. Carrier induced epitopic suppression of antibody responses induced by virus-like particles is a dynamic phenomenon caused by carrier-specific antibodies. Vaccine28(33), 5503–5512 (2010).
  • Brokstad KA, Cox RJ, Eriksson JC, Olofsson J, Jonsson R, Davidsson A. High prevalence of influenza specific antibody secreting cells in nasal mucosa. Scand. J. Immunol.54(1–2), 243–247 (2001).
  • Peduzzi E, Westerfeld N, Zurbriggen R, Pluschke G, Daubenberger CA. Contribution of influenza immunity and virosomal-formulated synthetic peptide to cellular immune responses in a Phase I subunit malaria vaccine trial. Clin. Immunol.127(2), 188–197 (2008).
  • Van der Wielen M, Vertruyen A, Froesner G et al. Immunogenicity and safety of a pediatric dose of a virosome-adjuvanted hepatitis A vaccine: a controlled trial in children aged 1–16 years. Pediatr. Infect. Dis. J.26(8), 705–710 (2007).
  • Bovier PA. Recent advances with a virosomal hepatitis A vaccine. Expert. Opin. Biol. Ther.8(8), 1177–1185 (2008).
  • Dagan R, Amir J, Livni G et al. Concomitant administration of a virosome-adjuvanted hepatitis a vaccine with routine childhood vaccines at age twelve to fifteen months: a randomized controlled trial. Pediatr. Infect. Dis. J.26(9), 787–793 (2007).
  • Holzer BR, Hatz C, Schmidt-Sissolak D, Gluck R, Althaus B, Egger M. Immunogenicity and adverse effects of inactivated virosome versus alum-adsorbed hepatitis A vaccine: a randomized controlled trial. Vaccine14(10), 982–986 (1996).
  • Clarke PD, Adams P, Ibanez R, Herzog C. Rate, intensity, and duration of local reactions to a virosome-adjuvanted vs. an aluminium-adsorbed hepatitis A vaccine in UK travellers. Travel Med. Infect. Dis.4(6), 313–318 (2006).
  • Bovier PA, Farinelli T, Loutan L. Interchangeability and tolerability of a virosomal and an aluminum-adsorbed hepatitis A vaccine. Vaccine23(19), 2424–2429 (2005).
  • Wilschut J. Influenza vaccines: the virosome concept. Immunol. Lett.122(2), 118–121 (2009).
  • Calcagnile S, Zuccotti GV. The virosomal adjuvanted influenza vaccine. Expert. Opin. Biol. Ther.10(2), 191–200 (2010).
  • Kursteiner O, Moser C, Lazar H, Durrer P. Inflexal V – the influenza vaccine with the lowest ovalbumin content. Vaccine24(44–46), 6632–6635 (2006).
  • Gluck R. Intranasal immunization against influenza. J. Aerosol Med.15(2), 221–228 (2002).
  • 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).
  • de Bruijn IA, Nauta J, Gerez L, Palache AM. The virosomal influenza vaccine Invivac: immunogenicity and tolerability compared to an adjuvanted influenza vaccine (Fluad) in elderly subjects. Vaccine24(44–46), 6629–6631 (2006).
  • de Bruijn I, Meyer I, Gerez L, Nauta J, Giezeman K, Palache B. Antibody induction by virosomal, MF59-adjuvanted, or conventional influenza vaccines in the elderly. Vaccine26(1), 119–127 (2007).
  • Westerfeld N, Pluschke G, Zurbriggen R. Optimized malaria-antigens delivered by immunostimulating reconstituted influenza virosomes. Wien. Klin. Wochenschr.118(19–20 Suppl. 3), 50–57 (2006).
  • Cavanagh DR, Remarque EJ, Sauerwein RW, Hermsen CC, Luty AJ. Influenza virosomes: a flu jab for malaria? Trends Parasitol.24(9), 382–385 (2008).
  • Okitsu SL, Silvie O, Westerfeld N et al. A virosomal malaria peptide vaccine elicits a long-lasting sporozoite-inhibitory antibody response in a Phase 1a clinical trial. PLoS ONE2(12), e1278 (2007).
  • Genton B, Aebi T, Abdallah MS et al. A phase 1b double-blind randomized controlled age-deescalting trial of two virosome formulated anti-malaria vaccine components administered in combination to healthy semi-immune Tanzanian adults and children. Presented at: 59th Annual Meeting of the American Society of Tropical Medicine and Hygiene. Atlanta, GA, USA, 3–7 November 2010.
  • Murphy CG, Fornier M. HER2-positive breast cancer: beyond trastuzumab. Oncology (Williston Park)24(5), 410–415 (2010).
  • Tudor D, Derrien M, Diomede L et al. HIV-1 gp41-specific monoclonal mucosal IgAs derived from highly exposed but IgG-seronegative individuals block HIV-1 epithelial transcytosis and neutralize CD4(+) cell infection: an IgA gene and functional analysis. Mucosal Immunol.2(5), 412–426 (2009).
  • De Bernardis F, Liu H, O’Mahony R et al. Human domain antibodies against virulence traits of Candida albicans inhibit fungus adherence to vaginal epithelium and protect against experimental vaginal candidiasis. J. Infect. Dis.195(1), 149–157 (2007).
  • Hunziker IP, Zurbriggen R, Glueck R et al. Perspectives: towards a peptide-based vaccine against hepatitis C virus. Mol. Immunol.38(6), 475–484 (2001).
  • De Bernardis F, Boccanera M, Adriani D, Girolamo A, Cassone A. Intravaginal and intranasal immunizations are equally effective in inducing vaginal antibodies and conferring protection against vaginal candidiasis. Infect. Immun.70(5), 2725–2729 (2002).

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