Influence of antigen conformation and mode of presentation on the antibody and protective responses against human respiratory syncytial virus: relevance for vaccine development

References

• Collins PL, Melero JA. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 2011;162:80–99.
   PubMed Web of Science ®Google Scholar
• Collins PL, Fearns R, Graham BS. Respiratory syncytial virus: virology, reverse genetics, and pathogenesis of disease. CurrTop Microbiol Immunol. 2013;372:3–38.
   PubMed Web of Science ®Google Scholar
• Hall CB, Weinberg GA, Iwane MK, et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009;360:588–598.
   PubMed Web of Science ®Google Scholar
• Nair H, Nokes DJ, Gessner BD, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet. 2010;375:1545–1555.
   PubMed Web of Science ®Google Scholar
• Hall CB, Powell KR, Macdonald NE, et al. Respiratory syncytial viral infection in children with compromised immune function. N Engl J Med. 1986;315:77–81.
   PubMed Web of Science ®Google Scholar
• Falsey AR, Hennessey PA, Formica MA, et al. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med. 2005;352:1749–1759.
   PubMed Web of Science ®Google Scholar
• Dowell SF, Anderson LJ, Gary HE Jr., et al. Respiratory syncytial virus is an important cause of community-acquired lower respiratory infection among hospitalized adults. J Infect Dis. 1996;174:456–462.
   PubMed Web of Science ®Google Scholar
• Drysdale SB, Sande CJ, Green CA, et al. RSV vaccine use - the missing data. Expert Rev Vaccines. 2016;15:149–152.
   PubMed Web of Science ®Google Scholar
• Mejias A, Ramilo O. Review of palivizumab in the prophylaxis of respiratory syncytial virus (RSV) in high-risk infants. Biologics. 2008;2:433–439.
   PubMedGoogle Scholar
• Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. The IMpact-RSV study group. Pediatrics. 1998;102:531–537.
   PubMed Web of Science ®Google Scholar
• Johnson S, Oliver C, Prince GA, et al. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J Infect Dis. 1997;176:1215–1224.
   PubMed Web of Science ®Google Scholar
• Simoes EA, Groothuis JR, Carbonell-Estrany X, et al. Palivizumab prophylaxis, respiratory syncytial virus, and subsequent recurrent wheezing. J Pediatr. 2007;151:34–42.
   PubMed Web of Science ®Google Scholar
• Kapikian AZ, Mitchell RH, Chanock RM, et al. An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol. 1969;89:405–421.
   PubMed Web of Science ®Google Scholar
• Fulginiti VA, Eller JJ, Sieber OF, et al. Respiratory virus immunization. I. A field trial of two inactivated respiratory virus vaccines; an aqueous trivalent parainfluenza virus vaccine and an alum-precipitated respiratory syncytial virus vaccine. Am J Epidemiol. 1969;89:435–448.
   PubMed Web of Science ®Google Scholar
• Kim HW, Canchola JG, Brandt CD, et al. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol. 1969;89:422–434.
   PubMed Web of Science ®Google Scholar
• Chin J, Magoffin RL, Shearer LA, et al. Field evaluation of a respiratory syncytial virus vaccine and a trivalent parainfluenza virus vaccine in a pediatric population. Am J Epidemiol. 1969;89:449–463.
   PubMed Web of Science ®Google Scholar
• Murphy BR, Prince GA, Walsh EE, et al. Dissociation between serum neutralizing and glycoprotein antibody responses of infants and children who received inactivated respiratory syncytial virus vaccine. J Clin Microbiol. 1986;24:197–202.
   PubMed Web of Science ®Google Scholar
• Polack FP, Teng MN, Collins PL, et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J Exp Med. 2002;196:859–865.
   PubMed Web of Science ®Google Scholar
• Delgado MF, Coviello S, Monsalvo AC, et al. Lack of antibody affinity maturation due to poor toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat Med. 2009;15:34–41.
   PubMed Web of Science ®Google Scholar
• Graham BS, Henderson GS, Tang YW, et al. Priming immunization determines T helper cytokine mRNA expression patterns in lungs of mice challenged with respiratory syncytial virus. J Immunol. 1993;151:2032–2040.
   PubMed Web of Science ®Google Scholar
• Wright PF, Karron RA, Belshe RB, et al. The absence of enhanced disease with wild type respiratory syncytial virus infection occurring after receipt of live, attenuated, respiratory syncytial virus vaccines. Vaccine. 2007;25:7372–7378.
   PubMed Web of Science ®Google Scholar
• Morrison TG, Walsh EE. Subunit and virus-like particle vaccine approaches for respiratory syncytial virus. CurrTop Microbiol Immunol. 2013;372:285–306.
   PubMed Web of Science ®Google Scholar
• Hall CB, Walsh EE, Long CE, et al. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis. 1991;163:693–698.
   PubMed Web of Science ®Google Scholar
• Glezen WP, Taber LH, Frank AL, et al. Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child. 1986;140:543–546.
   PubMedGoogle Scholar
• Falsey AR, Walsh EE. Relationship of serum antibody to risk of respiratory syncytial virus infection in elderly adults. J Infect Dis. 1998;177:463–466.
   PubMed Web of Science ®Google Scholar
• Connors M, Collins PL, Firestone CY, et al. Respiratory syncytial virus (RSV) F, G, M2 (22K), and N proteins each induce resistance to RSV challenge, but resistance induced by M2 and N proteins is relatively short-lived. J Virol. 1991;65:1634–1637.
   PubMed Web of Science ®Google Scholar
• Stott EJ, Taylor G, Ball LA, et al. Immune and histopathological responses in animals vaccinated with recombinant vaccinia viruses that express individual genes of human respiratory syncytial virus. J Virol. 1987;61:3855–3861.
   PubMed Web of Science ®Google Scholar
• Olmsted RA, Elango N, Prince GA, et al. Expression of the F glycoprotein of respiratory syncytial virus by a recombinant vaccinia virus: comparison of the individual contributions of the F and G glycoproteins to host immunity. Proc Natl Acad Sci U.S.A. 1986;83:7462–7466.
   PubMed Web of Science ®Google Scholar
• Kasel JA, Walsh EE, Frank AL, et al. Relation of serum antibody to glycoproteins of respiratory syncytial virus with immunity to infection in children. Viral Immunol. 1987;1:199–205.
   PubMedGoogle Scholar
• Hallak LK, Spillmann D, Collins PL, et al. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol. 2000;74:10508–10513.
   PubMed Web of Science ®Google Scholar
• Martinez I, Melero JA. Binding of human respiratory syncytial virus to cells: implication of sulfated cell surface proteoglycans. J Gen Virol. 2000;81:2715–2722.
   PubMed Web of Science ®Google Scholar
• Johnson SM, McNally BA, Ioannidis I, et al. Respiratory syncytial virus uses CX3CR1 as a receptor on primary human airway epithelial cultures. PLoS Pathog. 2015;11:e1005318.
   PubMed Web of Science ®Google Scholar
• Mas V, Melero JA. Entry of enveloped viruses into host cells: membrane fusion. Subcell Biochem. 2013;68:467–487.
   PubMedGoogle Scholar
• Gonzalez-Reyes L, Ruiz-Arguello MB, Garcia-Barreno B, et al. Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc Natl Acad Sci U.S.A. 2001;98:9859–9864.
   PubMed Web of Science ®Google Scholar
• Lamb RA. Paramyxovirus fusion: a hypothesis for changes. Virology. 1993;197:1–11.
   PubMed Web of Science ®Google Scholar
• Swanson KA, Settembre EC, Shaw CA, et al. Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc Natl Acad Sci U.S.A. 2011;108:9619–9624.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Yang Y, Graham BS, et al. Structure of the respiratory syncytial virus fusion glycoprotein in the post-fusion conformation reveals preservation of neutralizing epitopes. J Virol. 2011;85:7788–7796.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Chen M, Leung S, et al. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science. 2013;340:1113–1117.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Chen M, Joyce MG, et al. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science. 2013;342:592–598.
   PubMed Web of Science ®Google Scholar
• Stewart-Jones GB, Thomas PV, Chen M, et al. A cysteine zipper stabilizes a pre-fusion F glycoprotein vaccine for respiratory syncytial virus. PLoS One. 2015;10:e0128779.
   PubMed Web of Science ®Google Scholar
• Krarup A, Truan D, Furmanova-Hollenstein P, et al. A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism. Nat Commun. 2015;6:8143.
   PubMed Web of Science ®Google Scholar
• Calder LJ, Gonzalez-Reyes L, Garcia-Barreno B, et al. Electron microscopy of the human respiratory syncytial virus fusion protein and complexes that it forms with monoclonal antibodies. Virology. 2000;271:122–131.
   PubMed Web of Science ®Google Scholar
• Corti D, Bianchi S, Vanzetta F, et al. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature. 2013;501:439–443.
   PubMed Web of Science ®Google Scholar
• Wu SJ, Schmidt A, Beil EJ, et al. Characterization of the epitope for anti-human respiratory syncytial virus F protein monoclonal antibody 101F using synthetic peptides and genetic approaches. J Gen Virol. 2007;88:2719–2723.
   PubMed Web of Science ®Google Scholar
• Gilman MS, Moin SM, Mas V, et al. Characterization of a prefusion-specific antibody that recognizes a quaternary, cleavage-dependent epitope on the RSV fusion glycoprotein. PLoS Pathog. 2015;11:e1005035.
   PubMed Web of Science ®Google Scholar
• Melero JA, Moore ML. Influence of respiratory syncytial virus strain differences on pathogenesis and immunity. CurrTop Microbiol Immunol. 2013;372:59–82.
   PubMed Web of Science ®Google Scholar
• Sastre P, Melero JA, Garcia-Barreno B, et al. Comparison of affinity chromatography and adsorption to vaccinia virus recombinant infected cells for depletion of antibodies directed against respiratory syncytial virus glycoproteins present in a human immunoglobulin preparation. J Med Virol. 2005;76:248–255.
   PubMed Web of Science ®Google Scholar
• Magro M, Mas V, Chappell K, et al. Neutralizing antibodies against the preactive form of respiratory syncytial virus fusion protein offer unique possibilities for clinical intervention. Proc Natl Acad Sci U.S.A. 2012;109:3089–3094.
   PubMed Web of Science ®Google Scholar
• Ngwuta JO, Chen M, Modjarrad K, et al. Prefusion F-specific antibodies determine the magnitude of RSV neutralizing activity in human sera. Sci Transl Med. 2015;7:309ra162.
   PubMed Web of Science ®Google Scholar
• Kwakkenbos MJ, Diehl SA, Yasuda E, et al. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nat Med. 2010;16:123–128.
   PubMed Web of Science ®Google Scholar
• Graham BS, Modjarrad K, McLellan JS. Novel antigens for RSV vaccines. Curr Opin Immunol. 2015;35:30–38.
   PubMed Web of Science ®Google Scholar
• Garcia-Barreno B, Palomo C, Penas C, et al. Marked differences in the antigenic structure of human respiratory syncytial virus F and G glycoproteins. J Virol. 1989;63:925–932.
   PubMed Web of Science ®Google Scholar
• Beeler JA, Van Wyke CK. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J Virol. 1989;63:2941–2950.
   PubMed Web of Science ®Google Scholar
• Arbiza J, Taylor G, Lopez JA, et al. Characterization of two antigenic sites recognized by neutralizing monoclonal antibodies directed against the fusion glycoprotein of human respiratory syncytial virus. J Gen Virol. 1992;73(Pt 9):2225–2234.
   PubMed Web of Science ®Google Scholar
• Lopez JA, Andreu D, Carreno C, et al. Conformational constraints of conserved neutralizing epitopes from a major antigenic area of human respiratory syncytial virus fusion glycoprotein. J Gen Virol. 1993;74(Pt 12):2567–2577.
   PubMed Web of Science ®Google Scholar
• Toiron C, Lopez JA, Rivas G, et al. Conformational studies of a short linear peptide corresponding to a major conserved neutralizing epitope of human respiratory syncytial virus fusion glycoprotein. Biopolymers. 1996;39:537–548.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Chen M, Kim A, et al. Structural basis of respiratory syncytial virus neutralization by motavizumab. Nat Struct Mol Biol. 2010;17:248–250.
   PubMed Web of Science ®Google Scholar
• McLellan JS, Correia BE, Chen M, et al. Design and characterization of epitope-scaffold immunogens that present the motavizumab epitope from respiratory syncytial virus. J Mol Biol. 2011;409:853–866.
   PubMed Web of Science ®Google Scholar
• Correia BE, Bates JT, Loomis RJ, et al. Proof of principle for epitope-focused vaccine design. Nature. 2014;507:201–206.
   PubMed Web of Science ®Google Scholar
• Schickli JH, Whitacre DC, Tang RS, et al. Palivizumab epitope-displaying virus-like particles protect rodents from RSV challenge. J Clin Invest. 2015;125:1637–1647.
   PubMed Web of Science ®Google Scholar
• Smith G, Raghunandan R, Wu Y, et al. Respiratory syncytial virus fusion glycoprotein expressed in insect cells form protein nanoparticles that induce protective immunity in cotton rats. PLoS One. 2012;7:e50852.
   PubMed Web of Science ®Google Scholar
• Glenn GM, Smith G, Fries L, et al. Safety and immunogenicity of a Sf9 insect cell-derived respiratory syncytial virus fusion protein nanoparticle vaccine. Vaccine. 2013;31:524–532.
   PubMed Web of Science ®Google Scholar
• Glenn GM, Fries LF, Thomas DN, et al. A randomized, blinded, controlled, dose-ranging study of a respiratory syncytial virus recombinant fusion (F) nanoparticle vaccine in healthy women of childbearing age. J Infect Dis. 2015;213:411–422.
   PubMed Web of Science ®Google Scholar
• Moss B. Reflections on the early development of poxvirus vectors. Vaccine. 2013;31:4220–4222.
   PubMed Web of Science ®Google Scholar
• Bembridge GP, Lopez JA, Bustos R, et al. Priming with a secreted form of the fusion protein of respiratory syncytial virus (RSV) promotes interleukin-4 (IL-4) and IL-5 production but not pulmonary eosinophilia following RSV challenge. J Virol. 1999;73:10086–10094.
   PubMed Web of Science ®Google Scholar
• Liang B, Surman S, Amaro-Carambot E, et al. Enhanced neutralizing antibody response induced by respiratory syncytial virus Prefusion F protein expressed by a vaccine candidate. J Virol. 2015;89:9499–9510.
   PubMed Web of Science ®Google Scholar
• Swanson KA, Balabanis K, Xie Y, et al. A monomeric uncleaved respiratory syncytial virus F antigen retains prefusion-specific neutralizing epitopes. J Virol. 2014;88:11802–11810.
   PubMed Web of Science ®Google Scholar
• Meier S, Guthe S, Kiefhaber T, et al. Foldon, the natural trimerization domain of T4 fibritin, dissociates into a monomeric A-state form containing a stable beta-hairpin: atomic details of trimer dissociation and local beta-hairpin stability from residual dipolar couplings. J Mol Biol. 2004;344:1051–1069.
   PubMed Web of Science ®Google Scholar
• Rigter A, Widjaja I, Versantvoort H, et al. A protective and safe intranasal RSV vaccine based on a recombinant prefusion-like form of the F protein bound to bacterium-like particles. PLoS One. 2013;8:e71072.
   PubMed Web of Science ®Google Scholar
• McGinnes LW, Gravel KA, Finberg RW, et al. Assembly and immunological properties of newcastle disease virus-like particles containing the respiratory syncytial virus F and G proteins. J Virol. 2011;85:366–377.
   PubMed Web of Science ®Google Scholar
• McGinnes CL, Schmidt MR, Kenward SA, et al. Murine immune responses to virus-like particle-associated pre- and postfusion forms of the respiratory syncytial virus F protein. J Virol. 2015;89:6835–6847.
   PubMed Web of Science ®Google Scholar
• Cullen LM, Blanco JC, Morrison TG. Cotton rat immune responses to virus-like particles containing the pre-fusion form of respiratory syncytial virus fusion protein. J Transl Med. 2015;13:350.
   PubMed Web of Science ®Google Scholar
• Jardetzky TS, Lamb RA. Activation of paramyxovirus membrane fusion and virus entry. Curr Opin Virol. 2014;5:24–33.
   PubMed Web of Science ®Google Scholar
• Melero JA, Mas V. The pneumovirinae fusion (F) protein: a common target for vaccines and antivirals. Virus Res. 2015;209:128–135.
   PubMed Web of Science ®Google Scholar
• Battles MB, Langedijk JP, Furmanova-Hollenstein P, et al. Molecular mechanism of respiratory syncytial virus fusion inhibitors. Nat Chem Biol. 2015;12:87–93.
   PubMed Web of Science ®Google Scholar
• Jaberolansar N, Toth I, Young PR, et al. Recent advances in the development of subunit-based RSV vaccines. Expert Rev Vaccines. 2016;15:53–68.
   PubMed Web of Science ®Google Scholar
• Yassine HM, Boyington JC, McTamney PM, et al. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med. 2015;21:1065–1070.
   PubMed Web of Science ®Google Scholar
• Karron RA, Buchholz UJ, Collins PL. Live-attenuated respiratory syncytial virus vaccines. CurrTop Microbiol Immunol. 2013;372:259–284.
   PubMed Web of Science ®Google Scholar
• Karron RA, Luongo C, Thumar B, et al. A gene deletion that up-regulates viral gene expression yields an attenuated RSV vaccine with improved antibody responses in children. Sci Transl Med. 2015;7:312ra175.
   PubMed Web of Science ®Google Scholar
• Boyoglu-Barnum S, Todd SO, Chirkova T, et al. An anti-G protein monoclonal antibody treats RSV disease more effectively than an anti-F monoclonal antibody in BALB/c mice. Virology. 2015;483:117–125.
   PubMed Web of Science ®Google Scholar
• Jorquera PA, Anderson L, Tripp RA. Understanding respiratory syncytial virus (RSV) vaccine development and aspects of disease pathogenesis. Expert Rev Vaccines. 2016;15:173–187.
   PubMed Web of Science ®Google Scholar
• Hultberg A, Temperton NJ, Rosseels V, et al. Llama-derived single domain antibodies to build multivalent, superpotent and broadened neutralizing antiviral molecules. PLoS One. 2011;6:e17665.
   PubMed Web of Science ®Google Scholar