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Reviews

Strategies towards universal pandemic influenza vaccines

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Pages 215-225 | Received 21 Apr 2015, Accepted 29 Oct 2015, Published online: 05 Dec 2015

References

  • Papers of special note have been highlighted as:
  • • of interest
  • •• of considerable interest
  • Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol. 2014;385:359–375.
  • Kilbourne ED. Influenza pandemics of the 20th century. Emerg Infect Dis. 2006;12:9–14.
  • Webster RG, Peiris M, Chen H, et al. H5N1 outbreaks and enzootic influenza. Emerg Infect Dis. 2006;12:3–8.
  • Widmer N, Meylan P, Ivanyuk A, et al. Oseltamivir in seasonal, avian H5N1 and pandemic 2009 A/H1N1 influenza: pharmacokinetic and pharmacodynamic characteristics. Clin Pharmacokinet. 2010;49:741–765.
  • Prieto-Lara E, Llanos-Mendez A. Safety and immunogenicity of prepandemic H5N1 influenza vaccines: a systematic review of the literature. Vaccine. 2010;28:4328–4334.
  • Luke CJ, Subbarao K. Vaccines for pandemic influenza. Emerg Infect Dis. 2006;12:66–72.
  • Burton DR, Poignard P, Stanfield RL, et al. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science. 2012;337:183–186.
  • Rabadan R, Levine AJ, Krasnitz M. Non-random reassortment in human influenza A viruses. Influenza Other Respir Viruses. 2008;2:9–22.
  • Smith DJ, Lapedes AS, De Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science. 2004;305:371–376.
  • Plotkin JB, Dushoff J, Levin SA. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc Natl Acad Sci USA. 2002;99:6263–6268.
  • Yuen KY, Wong SS. Human infection by avian influenza A H5N1. Hong Kong Med J. 2005;11:189–199.
  • Skeik N, Jabr FI. Influenza viruses and the evolution of avian influenza virus H5N1. Int J Infect Dis. 2008;12:233–238.
  • Webster RG, Hulse-Post DJ, Sturm-Ramirez KM, et al. Changing epidemiology and ecology of highly pathogenic avian H5N1 influenza viruses. Avian Dis. 2007;51:269–272.
  • Shore DA, Yang H, Balish AL, et al. Structural and antigenic variation among diverse clade 2 H5N1 viruses. PLoS One. 2013;8:e75209.
  • Fidler DP, Gostin LO. The WHO pandemic influenza preparedness framework: a milestone in global governance for health. Jama. 2011;306:200–201.
  • Vemula SV, Ahi YS, Swaim AM, et al. Broadly protective adenovirus-based multivalent vaccines against highly pathogenic avian influenza viruses for pandemic preparedness. PLoS One. 2013;8:e62496.
  • Du N, Li W, Li Y, et al. Generation and evaluation of the trivalent inactivated reassortant vaccine using human, avian, and swine influenza A viruses. Vaccine. 2008;26:2912–2918.
  • Prabakaran M, He F, Meng T, et al. Neutralizing epitopes of influenza virus hemagglutinin: target for the development of a universal vaccine against H5N1 lineages. J Virol. 2010;84:11822–11830.
  • Treanor JJ, Schiff GM, Couch RB, et al. Dose-related safety and immunogenicity of a trivalent baculovirus-expressed influenza-virus hemagglutinin vaccine in elderly adults. J Infect Dis. 2006;193:1223–1228.
  • Ducatez MF, Bahl J, Griffin Y, et al. Feasibility of reconstructed ancestral H5N1 influenza viruses for cross-clade protective vaccine development. Proc Natl Acad Sci USA. 2011;108:349–354.
  • Krammer F, Palese P. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov. 2015;14:167–182.
  • Krammer F, Palese P, Steel J. Advances in universal influenza virus vaccine design and antibody mediated therapies based on conserved regions of the hemagglutinin. Curr Top Microbiol Immunol. 2015;386:301–321.
  • Giles BM, Ross TM. A computationally optimized broadly reactive antigen (COBRA) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets. Vaccine. 2011;29:3043–3054.
  • Giles BM, Bissel SJ, Dealmeida DR, et al. Antibody breadth and protective efficacy are increased by vaccination with computationally optimized hemagglutinin but not with polyvalent hemagglutinin-based H5N1 virus-like particle vaccines. Clin Vaccine Immunol. 2012;19:128–139.
  • Chen MW, Cheng TJ, Huang Y, et al. A consensus-hemagglutinin-based DNA vaccine that protects mice against divergent H5N1 influenza viruses. Proc Natl Acad Sci USA. 2008;105:13538–13543.
  • Laddy DJ, Yan J, Corbitt N, et al. Immunogenicity of novel consensus-based DNA vaccines against avian influenza. Vaccine. 2007;25:2984–2989.
  • He F, Prabakaran M, Rajesh Kumar S, et al. Monovalent H5 vaccine based on epitope-chimeric HA provides broad cross-clade protection against variant H5N1 viruses in mice. Antiviral Res. 2014;105:143–151.

• The manuscript provides a new efficient method for universal H5 vaccine production.

  • Prabakaran M, Prabhu N, He F, et al. Combination therapy using chimeric monoclonal antibodies protects mice from lethal H5N1 infection and prevents formation of escape mutants. PLoS One. 2009;4:e5672.
  • He F, Soejoedono RD, Murtini S, et al. Complementary monoclonal antibody-based dot ELISA for universal detection of H5 avian influenza virus. BMC Microbiol. 2010;10:330.
  • Ho HT, Qian HL, He F, et al. Rapid detection of H5N1 subtype influenza viruses by antigen capture enzyme-linked immunosorbent assay using H5- and N1-specific monoclonal antibodies. Clin Vaccine Immunol. 2009;16:726–732.
  • Prabakaran M, Ho HT, Prabhu N, et al. Development of epitope-blocking ELISA for universal detection of antibodies to human H5N1 influenza viruses. PLoS One. 2009;4:e4566.
  • Kaverin NV, Rudneva IA, Ilyushina NA, et al. Structure of antigenic sites on the haemagglutinin molecule of H5 avian influenza virus and phenotypic variation of escape mutants. J Gen Virol. 2002;83:2497–2505.
  • Kumar SR, Prabakaran M, Ashok Raj KV, et al. Amino acid substitutions improve the immunogenicity of H7N7HA protein and protect mice against lethal H7N7 viral challenge. PLoS One. 2015;10:e0128940.
  • Medina RA, Stertz S, Manicassamy B, et al. Glycosylations in the globular head of the hemagglutinin protein modulate the virulence and antigenic properties of the H1N1 influenza viruses. Sci Transl Med. 2013;5:187ra70.
  • Brandenburg B, Koudstaal W, Goudsmit J, et al. Mechanisms of hemagglutinin targeted influenza virus neutralization. PLoS One. 2013;8:e80034.
  • Xu K, Ling ZY, Sun L, et al. Broad humoral and cellular immunity elicited by a bivalent DNA vaccine encoding HA and NP genes from an H5N1 virus. Viral Immunol. 2011;24:45–56.
  • Chen GL, Subbarao K. Attacking the flu: neutralizing antibodies may lead to ‘universal’ vaccine. Nat Med. 2009;15:1251–1252.

•• The paper reveals the universal antibodies and epitopes, which enlightens future universal vaccine design.

  • Oxford JS, Schild GC. Immunological and physicochemical studies of influenza matrix (M) polypeptides. Virology. 1976;74:394–402.
  • Deng L, Cho KJ, Fiers W, et al. M2e-based universal influenza A vaccines. Vaccines. 2015;3:105–136.
  • Wu F, Huang JH, Yuan XY, et al. Characterization of immunity induced by M2e of influenza virus. Vaccine. 2007;25:8868–8873.
  • Lu Y, Welsh JP, Swartz JR. Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines. Proc Natl Acad Sci USA. 2014;111:125–130.
  • Hashem AM. Prospects of HA-based universal influenza vaccine. Biomed Res Int. 2015;2015:414637.
  • Zheng M, Luo J, Chen Z. Development of universal influenza vaccines based on influenza virus M and NP genes. Infection. 2014;42:251–262.
  • Heiny AT, Miotto O, Srinivasan KN, et al. Evolutionarily conserved protein sequences of influenza a viruses, avian and human, as vaccine targets. PLoS One. 2007;2:e1190.
  • Impagliazzo A, Milder F, Kuipers H, et al. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science. 2015;349(6254):1301–1306.
  • Li Z, Gabbard JD, Mooney A, et al. Single-dose vaccination of a recombinant parainfluenza virus 5 expressing NP from H5N1 virus provides broad immunity against influenza A viruses. J Virol. 2013;87:5985–5993.
  • Price GE, Lo CY, Misplon JA, et al. Mucosal immunization with a candidate universal influenza vaccine reduces virus transmission in a mouse model. J Virol. 2014;88:6019–6030.
  • Lillie PJ, Berthoud TK, Powell TJ, et al. Preliminary assessment of the efficacy of a T-cell-based influenza vaccine, MVA-NP+M1, in humans. Clin Infect Dis. 2012;55:19–25.
  • Shim BS, Choi YK, Yun CH, et al. Sublingual immunization with M2-based vaccine induces broad protective immunity against influenza. PLoS One. 2011;6:e27953.
  • He F, Madhan S, Kwang J. Baculovirus vector as a delivery vehicle for influenza vaccines. Expert Rev Vaccines. 2009;8:455–467.

•• A comprehensive review summarizes different types of baculovirus-expressed vaccines.

  • Yang DG, Chung YC, Lai YK, et al. Avian influenza virus hemagglutinin display on baculovirus envelope: cytoplasmic domain affects virus properties and vaccine potential. Mol Ther. 2007;15:989–996.
  • Hemann EA, Kang SM, Legge KL. Protective CD8 T cell-mediated immunity against influenza A virus infection following influenza virus-like particle vaccination. J Immunol. 2013;191:2486–2494.
  • Lu L, Yu L, Kwang J. Baculovirus surface-displayed hemagglutinin of H5N1 influenza virus sustains its authentic cleavage, hemagglutination activity, and antigenicity. Biochem Biophys Res Commun. 2007;358:404–409.
  • Tretyakova I, Pearce MB, Florese R, et al. Intranasal vaccination with H5, H7 and H9 hemagglutinins co-localized in a virus-like particle protects ferrets from multiple avian influenza viruses. Virology. 2013;442:67–73.
  • Prabakaran M, Meng T, He F, et al. Subcutaneous immunization with baculovirus surface-displayed hemagglutinin of pandemic H1N1 Influenza A virus induces protective immunity in mice. Clin Vaccine Immunol. 2011;18:1582–1585.
  • Prabakaran M, Kwang J. Recombinant baculovirus displayed vaccine: a novel tool for the development of a cross-protective influenza H5N1 vaccine. Bioengineered. 2013;5(1):45–48.
  • Syed Musthaq S, Kumar SR, Szyporta M, et al. Immunization with baculovirus displayed H6 hemagglutinin vaccine protects mice against lethal H6 influenza virus challenge. Antiviral Res. 2014;109:42–53.
  • Rajesh Kumar S, Syed Khader SM, Kiener TK, et al. Intranasal immunization of baculovirus displayed hemagglutinin confers complete protection against mouse adapted highly pathogenic H7N7 reassortant influenza virus. PLoS One. 2013;8:e63856.
  • Prabakaran M, Velumani S, He F, et al. Protective immunity against influenza H5N1 virus challenge in mice by intranasal co-administration of baculovirus surface-displayed HA and recombinant CTB as an adjuvant. Virology. 2008;380:412–420.
  • Prabakaran M, Madhan S, Prabhu N, et al. Gastrointestinal delivery of baculovirus displaying influenza virus hemagglutinin protects mice against heterologous H5N1 infection. J Virol. 2010;84:3201–3209.

• An interesting paper about oral vaccine against influenza, which is the trend in future.

  • Chua TH, Leung CY, Fang HE, et al. Evaluation of a subunit H5 vaccine and an inactivated H5N2 avian influenza marker vaccine in ducks challenged with Vietnamese H5N1 highly pathogenic avian influenza virus. Influenza Res Treat. 2010;2010:489213.
  • Prabakaran M, Rajesh Kumar S, Ashok Raj KV, et al. Cross-protective efficacy of baculovirus displayed hemagglutinin against highly pathogenic influenza H7 subtypes. Antiviral Res. 2014;109:149–159.
  • Abe T, Takahashi H, Hamazaki H, et al. Baculovirus induces an innate immune response and confers protection from lethal influenza virus infection in mice. J Immunol. 2003;171:1133–1139.
  • Sutter G, Staib C. Vaccinia vectors as candidate vaccines: the development of modified vaccinia virus Ankara for antigen delivery. Curr Drug Targets Infect Disord. 2003;3:263–271.
  • Verheust C, Goossens M, Pauwels K, et al. Biosafety aspects of modified vaccinia virus Ankara (MVA)-based vectors used for gene therapy or vaccination. Vaccine. 2012;30:2623–2632.
  • Altenburg AF, Kreijtz JH, De Vries RD, et al. Modified vaccinia virus ankara (MVA) as production platform for vaccines against influenza and other viral respiratory diseases. Viruses. 2014;6:2735–2761.
  • Price PJ, Torres-Dominguez LE, Brandmuller C, et al. Modified vaccinia virus Ankara: innate immune activation and induction of cellular signalling. Vaccine. 2013;31:4231–4234.
  • Prabakaran M, Leyrer S, He F, et al. Progress toward a universal H5N1 vaccine: a recombinant modified vaccinia virus Ankara-expressing trivalent hemagglutinin vaccine. PLoS One. 2014;9:e107316.

• The paper indicated the progress about a universal H5 vaccine production, which was constructed with multiple strategies stated in this review.

  • Boyd AC, Ruiz-Hernandez R, Peroval MY, et al. Towards a universal vaccine for avian influenza: protective efficacy of modified vaccinia virus Ankara and adenovirus vaccines expressing conserved influenza antigens in chickens challenged with low pathogenic avian influenza virus. Vaccine. 2013;31:670–675.
  • Florek NW, Weinfurter JT, Jegaskanda S, et al. Modified vaccinia virus Ankara encoding influenza virus hemagglutinin induces heterosubtypic immunity in macaques. J Virol. 2014;88:13418–13428.
  • Hessel A, Savidis-Dacho H, Coulibaly S, et al. MVA vectors expressing conserved influenza proteins protect mice against lethal challenge with H5N1, H9N2 and H7N1 viruses. PLoS One. 2014;9:e88340.
  • Redkiewicz P, Sirko A, Kamel KA, et al. Plant expression systems for production of hemagglutinin as a vaccine against influenza virus. Acta Biochim Pol. 2014;61:551–560.
  • Ward BJ, Landry N, Trepanier S, et al. Human antibody response to N-glycans present on plant-made influenza virus-like particle (VLP) vaccines. Vaccine. 2014;32:6098–6106.
  • Kim EH, Park HJ, Han GY, et al. Intranasal adenovirus-vectored vaccine for induction of long-lasting humoral immunity-mediated broad protection against influenza in mice. J Virol. 2014;88:9693–9703.
  • Ng P, Parks RJ, Cummings DT, et al. A high-efficiency Cre/loxP-based system for construction of adenoviral vectors. Hum Gene Ther. 1999;10:2667–2672.
  • Garcia-Arriaza J, Cepeda V, Hallengard D, et al. A novel poxvirus-based vaccine, MVA-CHIKV, is highly immunogenic and protects mice against chikungunya infection. J Virol. 2014;88:3527–3547.
  • Tripp RA, Tompkins SM. Virus-vectored influenza virus vaccines. Viruses. 2014;6:3055–3079.
  • Subbarao K, Joseph T. Scientific barriers to developing vaccines against avian influenza viruses. Nat Rev Immunol. 2007;7:267–278.

• The review lists current challenges faced in vaccine development against avian flu.

  • Manzoli L, Salanti G, De Vito C, et al. Immunogenicity and adverse events of avian influenza A H5N1 vaccine in healthy adults: multiple-treatments meta-analysis. Lancet Infect Dis. 2009;9:482–492.
  • Rose MA, Zielen S, Baumann U. Mucosal immunity and nasal influenza vaccination. Expert Rev Vaccines. 2012;11:595–607.
  • Magnusson KE, Stjernstrom I. Mucosal barrier mechanisms. Interplay between secretory IgA (SIgA), IgG and mucins on the surface properties and association of salmonellae with intestine and granulocytes. Immunology. 1982;45:239–248.
  • Schneider-Ohrum K, Giles BM, Weirback HK, et al. Adjuvants that stimulate TLR3 or NLPR3 pathways enhance the efficiency of influenza virus-like particle vaccines in aged mice. Vaccine. 2011;29:9081–9092.
  • Ribeiro CM, Schijns VE. Immunology of vaccine adjuvants. Methods Mol Biol. 2010;626:1–14.
  • Tamura S, Miyata K, Matsuo K, et al. Acceleration of influenza virus clearance by Th1 cells in the nasal site of mice immunized intranasally with adjuvant-combined recombinant nucleoprotein. J Immunol. 1996;156:3892–3900.
  • Guo L, Zheng M, Ding Y, et al. Protection against multiple influenza A virus subtypes by intranasal administration of recombinant nucleoprotein. Arch Virol. 2010;155:1765–1775.
  • Wang W, Huang B, Jiang T, et al. Maximal immune response and cross protection by influenza virus nucleoprotein derived from E. coli using an optimized formulation. Virology. 2014;468–470:265–273.
  • Eberly MD, Kader M, Hassan W, et al. Increased IL-15 production is associated with higher susceptibility of memory CD4 T cells to simian immunodeficiency virus during acute infection. J Immunol. 2009;182:1439–1448.
  • Oh S, Perera LP, Terabe M, et al. IL-15 as a mediator of CD4+ help for CD8+ T cell longevity and avoidance of TRAIL-mediated apoptosis. Proc Natl Acad Sci USA. 2008;105:5201–5206.
  • Oh S, Berzofsky JA, Burke DS, et al. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc Natl Acad Sci USA. 2003;100:3392–3397.
  • Poon LL, Leung YH, Nicholls JM, et al. Vaccinia virus-based multivalent H5N1 avian influenza vaccines adjuvanted with IL-15 confer sterile cross-clade protection in mice. J Immunol. 2009;182:3063–3071.
  • Muramatsu M, Yoshida R, Miyamoto H, et al. Heterosubtypic antiviral activity of hemagglutinin-specific antibodies induced by intranasal immunization with inactivated influenza viruses in mice. PLoS One. 2013;8:e71534.
  • Morokutti A, Muster T, Ferko B. Intranasal vaccination with a replication-deficient influenza virus induces heterosubtypic neutralising mucosal IgA antibodies in humans. Vaccine. 2014;32:1897–1900.
  • Prabakaran M, Kumar SR, Raj KV, et al. Cross-protective efficacy of baculovirus displayed hemagglutinin against highly pathogenic influenza H7 subtypes. Antiviral Res. 2014;109:149–159.
  • Quan FS, Compans RW, Kang SM. Oral vaccination with inactivated influenza vaccine induces cross-protective immunity. Vaccine. 2012;30:180–188.
  • Prabakaran M, Madhan S, Prabhu N, et al. Reverse micelle-encapsulated recombinant baculovirus as an oral vaccine against H5N1 infection in mice. Antiviral Res. 2010;86:180–187.
  • Adlhoch C, Gossner C, Koch G, et al. Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill. 2014;19(50):20996.
  • Ku KB, Park EH, Yum J, et al. Highly pathogenic avian influenza A(H5N8) virus from waterfowl, South Korea, 2014. Emerg Infect Dis. 2014;20:1587–1588.
  • Lee CC, Zhu H, Huang PY, et al. Emergence and evolution of avian H5N2 influenza viruses in chickens in Taiwan. J Virol. 2014;88:5677–5686.
  • Mao H, Guo B, Wang F, et al. A study of family clustering in two young girls with novel avian influenza A (H7N9) in Dongyang, Zhejiang Province, in 2014. J Clin Virol. 2015;63:18–24.
  • Hvistendahl M, Normile D, Cohen J. Influenza. Despite large research effort, H7N9 continues to baffle. Science. 2013;340:414–415.
  • Greenbaum A, Quinn C, Bailer J, et al. Investigation of an outbreak of variant influenza A(H3N2) virus infection associated with an agricultural fair-Ohio, August 2012. J Infect Dis. 2015;212:1592–1599.
  • Flannery B, Clippard J, Zimmerman RK, et al. Early estimates of seasonal influenza vaccine effectiveness - United States, January 2015. MMWR Morb Mortal Wkly Rep. 2015;64:10–15.
  • Van De Sandt CE, Kreijtz JH, De Mutsert G, et al. Human cytotoxic T lymphocytes directed to seasonal influenza A viruses cross-react with the newly emerging H7N9 virus. J Virol. 2014;88:1684–1693.
  • Bolton KJ, McCaw JM, Brown L, et al. Prior population immunity reduces the expected impact of CTL-inducing vaccines for pandemic influenza control. PLoS One. 2015;10:e0120138.
  • Herrmann VL, Hartmayer C, Planz O, et al. Cytotoxic T cell vaccination with PLGA microspheres interferes with influenza A virus replication in the lung and suppresses the infectious disease. J Control Release. 2015;216:121–131.
  • Chiu C, Wrammert J, Li GM, et al. Cross-reactive humoral responses to influenza and their implications for a universal vaccine. Ann N Y Acad Sci. 2013;1283:13–21.
  • Ramos I, Fernandez-Sesma A. Innate immunity to H5N1 influenza viruses in humans. Viruses. 2012;4:3363–3388.
  • Prescott S. Developmental immunology and vaccines: cellular immune development and future vaccine strategies. Expert Rev Vaccines. 2004;3:339–342.
  • Levine MM, Sztein MB. Vaccine development strategies for improving immunization: the role of modern immunology. Nat Immunol. 2004;5:460–464.
  • Kamlangdee A, Kingstad-Bakke B, Anderson TK, et al. Broad protection against avian influenza virus by using a modified vaccinia Ankara virus expressing a mosaic hemagglutinin gene. J Virol. 2014;88:13300–13309.
  • Valkenburg SA, Li OT, Mak PW, et al. IL-15 adjuvanted multivalent vaccinia-based universal influenza vaccine requires CD4+ T cells for heterosubtypic protection. Proc Natl Acad Sci USA. 2014;111:5676–5681.
  • Lang PO, Govind S, Mitchell WA, et al. Vaccine effectiveness in older individuals: what has been learned from the influenza-vaccine experience. Ageing Res Rev. 2011;10:389–395.
  • Moxon ER, Siegrist CA. The next decade of vaccines: societal and scientific challenges. Lancet. 2011;378:348–359.
  • Palache B, Krause R. Progress with human H5N1 vaccines: a perspective from industry. Expert Rev Vaccines. 2009;8:391–400.
  • Antrobus RD, Lillie PJ, Berthoud TK, et al. A T cell-inducing influenza vaccine for the elderly: safety and immunogenicity of MVA-NP+M1 in adults aged over 50 years. PLoS One. 2012;7:e48322.

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