Intranasal vaccination of recombinant H5N1 HA1 proteins fused with foldon and Fc induces strong mucosal immune responses with neutralizing activity: Implication for developing novel mucosal influenza vaccines

References

• Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998; 279:393-6; PMID:9430591; http://dx.doi.org/10.1126/science.279.5349.393
   PubMed Web of Science ®Google Scholar
• Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 2006; 312:404-10; PMID:16543414; http://dx.doi.org/10.1126/science.1124513
   PubMed Web of Science ®Google Scholar
• Du L, Leung VH, Zhang X, Zhou J, Chen M, He W, Zhang HY, Chan CC, Poon VK, Zhao G, et al. A recombinant vaccine of H5N1 HA1 fused with foldon and human IgG Fc induced complete cross-clade protection against divergent H5N1 viruses. PLoS One 2011; 6:e16555; PMID:21304591; http://dx.doi.org/10.1371/journal.pone.0016555
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, Sun S, Zhang X, Zhou X, Guo Y, Li Y, Zhou Y, Jiang S. A critical HA1 neutralizing domain of H5N1 influenza in an optimal conformation induces strong cross-protection. PLoS One 2013; 8:e53568; PMID:23320093; http://dx.doi.org/10.1371/journal.pone.0053568
   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 USA 2010; 107:18979-84; PMID:20956293; http://dx.doi.org/10.1073/pnas.1013387107
   PubMed Web of Science ®Google Scholar
• Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006; 6:148-58; PMID:16491139; http://dx.doi.org/10.1038/nri1777
   PubMed Web of Science ®Google Scholar
• Levine MM. Immunization against bacterial diseases of the intestine. J Pediatr Gastroenterol Nutr 2000; 31:336-55; PMID:11045827; http://dx.doi.org/10.1097/00005176-200010000-00003
   PubMed Web of Science ®Google Scholar
• Lamm ME. Interaction of antigens and antibodies at mucosal surfaces. Annu Rev Microbiol 1997; 51:311-40; PMID:9343353; http://dx.doi.org/10.1146/annurev.micro.51.1.311
   PubMed Web of Science ®Google Scholar
• Belshe RB, Mendelman PM, Treanor J, King J, Gruber WC, Piedra P, Bernstein DI, Hayden FG, Kotloff K, Zangwill K, et al. The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenzavirus vaccine in children. N Engl J Med 1998; 338:1405-12; PMID:9580647; http://dx.doi.org/10.1056/NEJM199805143382002
   PubMed Web of Science ®Google Scholar
• Wegmann F, Gartlan KH, Harandi AM, Brinckmann SA, Coccia M, Hillson WR, Kok WL, Cole S, Ho LP, Lambe T, et al. Polyethyleneimine is a potent mucosal adjuvant for viral glycoprotein antigens. Nat Biotechnol 2012; 30:883-8; PMID:22922673; http://dx.doi.org/10.1038/nbt.2344
   PubMed Web of Science ®Google Scholar
• Chuai X, Chen H, Wang W, Deng Y, Wen B, Ruan L, Tan W. Poly(I:C)/alum mixed adjuvant priming enhances HBV subunit vaccine-induced immunity in mice when combined with recombinant adenoviral-based HBV vaccine boosting. PLoS One 2013; 8:e54126; PMID:23335993; http://dx.doi.org/10.1371/journal.pone.0054126
   PubMed Web of Science ®Google Scholar
• Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011; 470:543-7; PMID:21350488; http://dx.doi.org/10.1038/nature09737
   PubMed Web of Science ®Google Scholar
• Yang X, Lee J, Mahony EM, Kwong PD, Wyatt R, Sodroski J. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J Virol 2002; 76:4634-42; PMID:11932429; http://dx.doi.org/10.1128/JVI.76.9.4634-4642.2002
   PubMed Web of Science ®Google Scholar
• Papanikolopoulou K, Forge V, Goeltz P, Mitraki A. Formation of highly stable chimeric trimers by fusion of an adenovirus fiber shaft fragment with the foldon domain of bacteriophage t4 fibritin. J Biol Chem 2004; 279:8991-8; PMID:14699113; http://dx.doi.org/10.1074/jbc.M311791200
   PubMed Web of Science ®Google Scholar
• Li Y, Du L, Qiu H, Zhao G, Wang L, Zhou Y, Jiang S, Gao J. A recombinant protein containing highly conserved hemagglutinin residues 81-122 of influenza H5N1 induces strong humoral and mucosal immune responses. Biosci Trends 2013; 7:129-37; PMID:23836036
   PubMed Web of Science ®Google Scholar
• Du L, Jin L, Zhao G, Sun S, Li J, Yu H, Li Y, Zheng BJ, Liddington RC, Zhou Y, et al. Identification and structural characterization of a broadly neutralizing antibody targeting a novel conserved epitope on the influenza virus H5N1 hemagglutinin. J Virol 2013; 87:2215-25; PMID:23221567; http://dx.doi.org/10.1128/JVI.02344-12
   PubMed Web of Science ®Google Scholar
• Zhang N, Jiang S, Du L. Current advancements and potential strategies in the development of MERS-CoV vaccines. Expert Rev Vaccines 2014; 13:761-74; PMID:24766432; http://dx.doi.org/10.1586/14760584.2014.912134
   PubMed Web of Science ®Google Scholar
• Zhang N, Tang J, Lu L, Jiang S, Du L. Receptor-binding domain-based subunit vaccines against MERS-CoV. Virus Res 2014; 202:151-9; PMID:25445336
   PubMed Web of Science ®Google Scholar
• He Y, Zhou Y, Liu S, Kou Z, Li W, Farzan M, Jiang S. Receptor-binding domain of SARS-CoV spike protein induces highly potent neutralizing antibodies: implication for developing subunit vaccine. Biochem Biophys Res Commun 2004; 324:773-81; PMID:15474494; http://dx.doi.org/10.1016/j.bbrc.2004.09.106
   PubMed Web of Science ®Google Scholar
• He Y, Lu H, Siddiqui P, Zhou Y, Jiang S. Receptor-binding domain of severe acute respiratory syndrome coronavirus spike protein contains multiple conformation-dependent epitopes that induce highly potent neutralizing antibodies. J Immunol 2005; 174:4908-15; PMID:15814718; http://dx.doi.org/10.4049/jimmunol.174.8.4908
   PubMed Web of Science ®Google Scholar
• Chen X, Lu L, Qi Z, Lu H, Wang J, Yu X, Chen Y, Jiang S. Novel recombinant engineered gp41 N-terminal heptad repeat trimers and their potential as anti-HIV-1 therapeutics or microbicides. J Biol Chem 2010; 285:25506-15; PMID:20538590; http://dx.doi.org/10.1074/jbc.M110.101170
   PubMed Web of Science ®Google Scholar
• Chen H, Xu X, Jones IM. Immunogenicity of the outer domain of a HIV-1 clade C gp120. Retrovirology 2007; 4:33; PMID:17509143; http://dx.doi.org/10.1186/1742-4690-4-33
   PubMed Web of Science ®Google Scholar
• Martyn JC, Cardin AJ, Wines BD, Cendron A, Li S, Mackenzie J, Powell M, Gowans EJ. Surface display of IgG Fc on baculovirus vectors enhances binding to antigen-presenting cells and cell lines expressing Fc receptors. Arch Virol 2009; 154:1129-38; PMID:19557497; http://dx.doi.org/10.1007/s00705-009-0423-8
   PubMed Web of Science ®Google Scholar
• Meier S, Guthe S, Kiefhaber T, Grzesiek S. Foldon, the natural trimerization domain of T4 fibritin, dissociates into a monomeric A-state form containing a stable β-hairpin: atomic details of trimer dissociation and local β-hairpin stability from residual dipolar couplings. J Mol Biol 2004; 344:1051-69; PMID:15544812; http://dx.doi.org/10.1016/j.jmb.2004.09.079
   PubMed Web of Science ®Google Scholar
• Steinhagen F, Kinjo T, Bode C, Klinman DM. TLR-based immune adjuvants. Vaccine 2011; 29:3341-55; PMID:20713100; http://dx.doi.org/10.1016/j.vaccine.2010.08.002
   PubMed Web of Science ®Google Scholar
• Beutler BA. TLRs and innate immunity. Blood 2009; 113:1399-407; PMID:18757776; http://dx.doi.org/10.1182/blood-2008-07-019307
   PubMed Web of Science ®Google Scholar
• Weldon WC, Wang BZ, Martin MP, Koutsonanos DG, Skountzou I, Compans RW. Enhanced immunogenicity of stabilized trimeric soluble influenza hemagglutinin. PLoS One 2010; 5:e12466; PMID:20824188; http://dx.doi.org/10.1371/journal.pone.0012466
   PubMed Web of Science ®Google Scholar
• Loureiro S, Ren J, Phapugrangkul P, Colaco CA, Bailey CR, Shelton H, Molesti E, Temperton NJ, Barclay WS, Jones IM. Adjuvant-free immunization with hemagglutinin-Fc fusion proteins as an approach to influenza vaccines. J Virol 2011; 85:3010-4; PMID:21191017; http://dx.doi.org/10.1128/JVI.01241-10
   PubMed Web of Science ®Google Scholar
• Wei CJ, Xu L, Kong WP, Shi W, Canis K, Stevens J, Yang ZY, Dell A, Haslam SM, Wilson IA, et al. Comparative efficacy of neutralizing antibodies elicited by recombinant hemagglutinin proteins from avian H5N1 influenza virus. J Virol 2008; 82:6200-8; PMID:18417563; http://dx.doi.org/10.1128/JVI.00187-08
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, He Y, Guo Y, Zheng BJ, Jiang S, Zhou Y. Receptor-binding domain of SARS-CoV spike protein induces long-term protective immunity in an animal model. Vaccine 2007; 25:2832-8; PMID:17092615; http://dx.doi.org/10.1016/j.vaccine.2006.10.031
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, Zhang X, Liu Z, Yu H, Zheng BJ, Zhou Y, Jiang S. Development of a safe and convenient neutralization assay for rapid screening of influenza HA-specific neutralizing monoclonal antibodies. Biochem Biophys Res Commun 2010; 397(3):580-5; PMID:20617558; http://dx.doi.org/10.1016/j.bbrc.2010.05.161
   PubMed Web of Science ®Google Scholar