Intranasal immunization with influenza antigens conjugated with cholera toxin subunit B stimulates broad spectrum immunity against influenza viruses

References

• Neumann G, Noda T, Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 2009; 459:931 - 9; http://dx.doi.org/10.1038/nature08157; PMID: 19525932
   PubMed Web of Science ®Google Scholar
• Li J, Arévalo MT, Zeng M. Engineering influenza viral vectors. Bioengineered 2013; 4:9 - 14; http://dx.doi.org/10.4161/bioe.21950; PMID: 22922205
   PubMed Web of Science ®Google Scholar
• Weaver EA, Rubrum AM, Webby RJ, Barry MA. Protection against divergent influenza H1N1 virus by a centralized influenza hemagglutinin. PLoS One 2011; 6:e18314; http://dx.doi.org/10.1371/journal.pone.0018314; PMID: 21464940
   PubMed Web of Science ®Google Scholar
• Roose K, Fiers W, Saelens X. Pandemic preparedness: toward a universal influenza vaccine. Drug News Perspect 2009; 22:80 - 92; http://dx.doi.org/10.1358/dnp.2009.22.2.1334451; PMID: 19330167
   PubMed Web of Science ®Google Scholar
• Pica N, Palese P. Toward a universal influenza virus vaccine: prospects and challenges. Annu Rev Med 2013; 64:189 - 202; http://dx.doi.org/10.1146/annurev-med-120611-145115; PMID: 23327522
   PubMed Web of Science ®Google Scholar
• Wang TT, Tan GS, Hai R, Pica N, Ngai L, Ekiert DC, Wilson IA, García-Sastre A, Moran TM, 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; 107:18979 - 84; http://dx.doi.org/10.1073/pnas.1013387107; PMID: 20956293
   PubMed Web of Science ®Google Scholar
• Hillaire ML, Osterhaus AD, Rimmelzwaan GF. Induction of virus-specific cytotoxic T lymphocytes as a basis for the development of broadly protective influenza vaccines. J Biomed Biotechnol 2011; 2011:939860; http://dx.doi.org/10.1155/2011/939860; PMID: 22007149
   PubMed Web of Science ®Google Scholar
• Staneková Z, Varečková E. Conserved epitopes of influenza A virus inducing protective immunity and their prospects for universal vaccine development. Virol J 2010; 7:351; http://dx.doi.org/10.1186/1743-422X-7-351; PMID: 21118546
   PubMed Web of Science ®Google Scholar
• Vergara-Alert J, Argilaguet JM, Busquets N, Ballester M, Martín-Valls GE, Rivas R, López-Soria S, Solanes D, Majó N, Segalés J, et al. Conserved synthetic peptides from the hemagglutinin of influenza viruses induce broad humoral and T-cell responses in a pig model. PLoS One 2012; 7:e40524; http://dx.doi.org/10.1371/journal.pone.0040524; PMID: 22815759
   PubMedGoogle Scholar
• Edwards MJ, Dimmock NJ. Two influenza A virus-specific Fabs neutralize by inhibiting virus attachment to target cells, while neutralization by their IgGs is complex and occurs simultaneously through fusion inhibition and attachment inhibition. Virology 2000; 278:423 - 35; http://dx.doi.org/10.1006/viro.2000.0631; PMID: 11118365
   PubMed Web of Science ®Google Scholar
• De Filette M, Ramne A, Birkett A, Lycke N, Löwenadler B, Min Jou W, Saelens X, Fiers W. The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine 2006; 24:544 - 51; http://dx.doi.org/10.1016/j.vaccine.2005.08.061; PMID: 16169634
   PubMed Web of Science ®Google Scholar
• De Filette M, Min Jou W, Birkett A, Lyons K, Schultz B, Tonkyro A, Resch S, Fiers W. Universal influenza A vaccine: optimization of M2-based constructs. Virology 2005; 337:149 - 61; http://dx.doi.org/10.1016/j.virol.2005.04.004; PMID: 15914228
   PubMed Web of Science ®Google Scholar
• 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 1999; 5:1157 - 63; http://dx.doi.org/10.1038/13484; PMID: 10502819
   PubMed Web of Science ®Google Scholar
• Saelens X, Vanlandschoot P, Martinet W, Maras M, Neirynck S, Contreras R, Fiers W, Jou WM. Protection of mice against a lethal influenza virus challenge after immunization with yeast-derived secreted influenza virus hemagglutinin. Eur J Biochem 1999; 260:166 - 75; http://dx.doi.org/10.1046/j.1432-1327.1999.00150.x; PMID: 10091596
   PubMedGoogle Scholar
• Holsinger LJ, Lamb RA. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 1991; 183:32 - 43; http://dx.doi.org/10.1016/0042-6822(91)90115-R; PMID: 2053285
   PubMed Web of Science ®Google Scholar
• Kim MC, Song JM, O E, Kwon YM, Lee YJ, Compans RW, Kang SM. Virus-like particles containing multiple M2 extracellular domains confer improved cross-protection against various subtypes of influenza virus. Mol Ther 2013; 21:485 - 92; http://dx.doi.org/10.1038/mt.2012.246; PMID: 23247101
   PubMed Web of Science ®Google Scholar
• Isaka M, Yasuda Y, Taniguchi T, Kozuka S, Matano K, Maeyama J, Morokuma K, Ohkuma K, Goto N, Tochikubo K. Mucosal and systemic antibody responses against an acellular pertussis vaccine in mice after intranasal co-administration with recombinant cholera toxin B subunit as an adjuvant. Vaccine 2003; 21:1165 - 73; http://dx.doi.org/10.1016/S0264-410X(02)00516-9; PMID: 12559794
   PubMed Web of Science ®Google Scholar
• Tochikubo K, Isaka M, Yasuda Y, Kozuka S, Matano K, Miura Y, Taniguchi T. Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses of mice to mucosally co-administered bovine serum albumin. Vaccine 1998; 16:150 - 5; http://dx.doi.org/10.1016/S0264-410X(97)00194-1; PMID: 9607023
   PubMed Web of Science ®Google Scholar
• Isaka M, Zhao Y, Nobusawa E, Nakajima S, Nakajima K, Yasuda Y, Matsui H, Hasegawa T, Maeyama J, Morokuma K, et al. Protective effect of nasal immunization of influenza virus hemagglutinin with recombinant cholera toxin B subunit as a mucosal adjuvant in mice. Microbiol Immunol 2008; 52:55 - 63; http://dx.doi.org/10.1111/j.1348-0421.2008.00010.x; PMID: 18380802
   PubMed Web of Science ®Google Scholar
• Seibert CW, Rahmat S, Krause JC, Eggink D, Albrecht RA, Goff PH, Krammer F, Duty JA, Bouvier NM, García-Sastre A, et al. Recombinant IgA is sufficient to prevent influenza virus transmission in guinea pigs. J Virol 2013; 87:7793 - 804; http://dx.doi.org/10.1128/JVI.00979-13; PMID: 23698296
   PubMed Web of Science ®Google Scholar
• Olvera-Gomez I, Hamilton SE, Xiao Z, Guimaraes CP, Ploegh HL, Hogquist KA, Wang L, Jameson SC. Cholera toxin activates nonconventional adjuvant pathways that induce protective CD8 T-cell responses after epicutaneous vaccination. Proc Natl Acad Sci U S A 2012; 109:2072 - 7; http://dx.doi.org/10.1073/pnas.1105771109; PMID: 22308317
   PubMed Web of Science ®Google Scholar
• Partidos CD, Beignon AS, Briand JP, Muller S. Modulation of immune responses with transcutaneously deliverable adjuvants. Vaccine 2004; 22:2385 - 90; http://dx.doi.org/10.1016/j.vaccine.2003.11.063; PMID: 15193399
   PubMed Web of Science ®Google Scholar
• Park MH, Chang J. Immunogenicity and protective efficacy of a dual subunit vaccine against respiratory syncytial virus and influenza virus. Immune Netw 2012; 12:261 - 8; http://dx.doi.org/10.4110/in.2012.12.6.261; PMID: 23396871
   PubMedGoogle Scholar
• Andrew DW, Hafner LM, Beagley KW, Timms P. Partial protection against chlamydial reproductive tract infection by a recombinant major outer membrane protein/CpG/cholera toxin intranasal vaccine in the guinea pig Chlamydia caviae model. J Reprod Immunol 2011; 91:9 - 16; http://dx.doi.org/10.1016/j.jri.2011.06.100; PMID: 21856018
   PubMed Web of Science ®Google Scholar
• Datta SK, Sabet M, Nguyen KP, Valdez PA, Gonzalez-Navajas JM, Islam S, Mihajlov I, Fierer J, Insel PA, Webster NJ, et al. Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax. Proc Natl Acad Sci U S A 2010; 107:10638 - 43; http://dx.doi.org/10.1073/pnas.1002348107; PMID: 20479237
   PubMed Web of Science ®Google Scholar
• Eliasson DG, El Bakkouri K, Schön K, Ramne A, Festjens E, Löwenadler B, Fiers W, Saelens X, Lycke N. CTA1-M2e-DD: a novel mucosal adjuvant targeted influenza vaccine. Vaccine 2008; 26:1243 - 52; http://dx.doi.org/10.1016/j.vaccine.2007.12.027; PMID: 18243429
   PubMed Web of Science ®Google Scholar
• Turley CB, Rupp RE, Johnson C, Taylor DN, Wolfson J, Tussey L, Kavita U, Stanberry L, Shaw A. Safety and immunogenicity of a recombinant M2e-flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine 2011; 29:5145 - 52; http://dx.doi.org/10.1016/j.vaccine.2011.05.041; PMID: 21624416
   PubMed Web of Science ®Google Scholar
• Alvarez P, Zylberman V, Ghersi G, Boado L, Palacios C, Goldbaum F, Mattion N. Tandem repeats of the extracellular domain of Matrix 2 influenza protein exposed in Brucella lumazine synthase decameric carrier molecule induce protection in mice. Vaccine 2013; 31:806 - 12; http://dx.doi.org/10.1016/j.vaccine.2012.11.072; PMID: 23246552
   PubMed Web of Science ®Google Scholar
• Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K, García-Sastre A, Palese P. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 2010; 1:e00018 - 10; http://dx.doi.org/10.1128/mBio.00018-10; PMID: 20689752
   PubMed Web of Science ®Google Scholar
• Bommakanti G, Citron MP, Hepler RW, Callahan C, Heidecker GJ, Najar TA, Lu X, Joyce JG, Shiver JW, Casimiro DR, et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc Natl Acad Sci U S A 2010; 107:13701 - 6; http://dx.doi.org/10.1073/pnas.1007465107; PMID: 20615991
   PubMed Web of Science ®Google Scholar
• Prabakaran M, Velumani S, He F, Karuppannan AK, Geng GY, Yin LK, Kwang J. 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 - 20; http://dx.doi.org/10.1016/j.virol.2008.08.002; PMID: 18786689
   PubMed Web of Science ®Google Scholar
• Guo L, Zheng M, Ding Y, Li D, Yang Z, Wang H, Chen Q, Sui Z, Fang F, Chen Z. Protection against multiple influenza A virus subtypes by intranasal administration of recombinant nucleoprotein. Arch Virol 2010; 155:1765 - 75; http://dx.doi.org/10.1007/s00705-010-0756-3; PMID: 20652335
   PubMed Web of Science ®Google Scholar
• Varecková E, Mucha V, Wharton SA, Kostolanský F. Inhibition of fusion activity of influenza A haemagglutinin mediated by HA2-specific monoclonal antibodies. Arch Virol 2003; 148:469 - 86; http://dx.doi.org/10.1007/s00705-002-0932-1; PMID: 12607099
   PubMed Web of Science ®Google Scholar
• Gocník M, Fislová T, Mucha V, Sládková T, Russ G, Kostolansky F, Varecková E. Antibodies induced by the HA2 glycopolypeptide of influenza virus haemagglutinin improve recovery from influenza A virus infection. J Gen Virol 2008; 89:958 - 67; http://dx.doi.org/10.1099/vir.0.83524-0; PMID: 18343837
   PubMed Web of Science ®Google Scholar
• Denkers EY, Badger CC, Ledbetter JA, Bernstein ID. Influence of antibody isotype on passive serotherapy of lymphoma. J Immunol 1985; 135:2183 - 6; PMID: 2862210
   PubMed Web of Science ®Google Scholar
• 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 2004; 172:5598 - 605; PMID: 15100303
   PubMed Web of Science ®Google Scholar
• Clegg CH, Roque R, Van Hoeven N, Perrone L, Baldwin SL, Rininger JA, Bowen RA, Reed SG. Adjuvant solution for pandemic influenza vaccine production. Proc Natl Acad Sci U S A 2012; 109:17585 - 90; http://dx.doi.org/10.1073/pnas.1207308109; PMID: 23045649
   PubMed Web of Science ®Google Scholar
• Petsch B, Schnee M, Vogel AB, Lange E, Hoffmann B, Voss D, Schlake T, Thess A, Kallen KJ, Stitz L, et al. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol 2012; 30:1210 - 6; http://dx.doi.org/10.1038/nbt.2436; PMID: 23159882
   PubMed Web of Science ®Google Scholar
• Jazi MH, Dabaghian M, Tebianian M, Gharagozlou MJ, Ebrahimi SM. In vivo electroporation enhances immunogenicity and protection against influenza A virus challenge of an M2e-HSP70c DNA vaccine. Virus Res 2012; 167:219 - 25; http://dx.doi.org/10.1016/j.virusres.2012.05.002; PMID: 22609252
   PubMed Web of Science ®Google Scholar
• Alexander J, Bilsel P, del Guercio MF, Stewart S, Marinkovic-Petrovic A, Southwood S, Crimi C, Vang L, Walker L, Ishioka G, et al. Universal influenza DNA vaccine encoding conserved CD4+ T cell epitopes protects against lethal viral challenge in HLA-DR transgenic mice. Vaccine 2010; 28:664 - 72; http://dx.doi.org/10.1016/j.vaccine.2009.10.103; PMID: 19895924
   PubMed Web of Science ®Google Scholar
• Wang W, Huang B, Jiang T, Wang X, Qi X, Gao Y, Tan W, Ruan L. Robust immunity and heterologous protection against influenza in mice elicited by a novel recombinant NP-M2e fusion protein expressed in E. coli. PLoS One 2012; 7:e52488; http://dx.doi.org/10.1371/journal.pone.0052488; PMID: 23285063
   PubMedGoogle Scholar
• Sendi P, Locher R, Bucheli B, Battegay M. Intranasal influenza vaccine in a working population. Clin Infect Dis 2004; 38:974 - 80; http://dx.doi.org/10.1086/386330; PMID: 15034829
   PubMed Web of Science ®Google Scholar
• Sendi P, Locher R, Bucheli B, Battegay M. The decision to get vaccinated against influenza. Am J Med 2004; 116:856 - 8; http://dx.doi.org/10.1016/j.amjmed.2004.02.023; PMID: 15178507
   PubMed Web of Science ®Google Scholar
• Bharati K, Ganguly NK. Cholera toxin: a paradigm of a multifunctional protein. Indian J Med Res 2011; 133:179 - 87; PMID: 21415492
   PubMed Web of Science ®Google Scholar
• Stål P, Befrits R, Rönnblom A, Danielsson A, Suhr O, Ståhlberg D, Brinkberg Lapidus A, Löfberg R. Clinical trial: the safety and short-term efficacy of recombinant cholera toxin B subunit in the treatment of active Crohn’s disease. Aliment Pharmacol Ther 2010; 31:387 - 95; http://dx.doi.org/10.1111/j.1365-2036.2009.04185.x; PMID: 19878149
   PubMed Web of Science ®Google Scholar
• Reed SG, Bertholet S, Coler RN, Friede M. New horizons in adjuvants for vaccine development. Trends Immunol 2009; 30:23 - 32; http://dx.doi.org/10.1016/j.it.2008.09.006; PMID: 19059004
   PubMed Web of Science ®Google Scholar
• Shim BS, Choi YK, Yun CH, Lee EG, Jeon YS, Park SM, Cheon IS, Joo DH, Cho CH, Song MS, et al. Sublingual immunization with M2-based vaccine induces broad protective immunity against influenza. PLoS One 2011; 6:e27953; http://dx.doi.org/10.1371/journal.pone.0027953; PMID: 22140491
   PubMed Web of Science ®Google Scholar
• Gerhard W, Mozdzanowska K, Furchner M, Washko G, Maiese K. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol Rev 1997; 159:95 - 103; http://dx.doi.org/10.1111/j.1600-065X.1997.tb01009.x; PMID: 9416505
   PubMed Web of Science ®Google Scholar
• Waffarn EE, Baumgarth N. Protective B cell responses to flu--no fluke!. J Immunol 2011; 186:3823 - 9; http://dx.doi.org/10.4049/jimmunol.1002090; PMID: 21422252
   PubMed Web of Science ®Google Scholar
• Swain SL, McKinstry KK, Strutt TM. Expanding roles for CD4⁺ T cells in immunity to viruses. Nat Rev Immunol 2012; 12:136 - 48; PMID: 22266691
   PubMed Web of Science ®Google Scholar
• Ilyushina NA, Khalenkov AM, Seiler JP, Forrest HL, Bovin NV, Marjuki H, Barman S, Webster RG, Webby RJ. Adaptation of pandemic H1N1 influenza viruses in mice. J Virol 2010; 84:8607 - 16; http://dx.doi.org/10.1128/JVI.00159-10; PMID: 20592084
   PubMed Web of Science ®Google Scholar