Novel recombinant DNA vaccine candidates for human respiratory syncytial virus: Preclinical evaluation of immunogenicity and protection efficiency

References

• Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O'Brien KL, Roca A, Wright PF, Bruce N, 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; 375:1545-55; PMID:20399493; https://doi.org/10.1016/S0140-6736(10)60206-1
   PubMed Web of Science ®Google Scholar
• Diez-Domingo J, Perez-Yarza EG, Melero JA, Sanchez-Luna M, Aguilar MD, Blasco AJ, Alfaro N, Lázaro P. Social, economic, and health impact of the respiratory syncytial virus: a systematic search. BMC Infect Dis 2014; 14:544; PMID:25358423; https://doi.org/10.1186/s12879-014-0544-x
   PubMed Web of Science ®Google Scholar
• Bont L, Versteegh J, Swelsen WT, Heijnen CJ, Kavelaars A, Brus F, Draaisma JM, Pekelharing-Berghuis M, van Diemen-Steenvoorde RA, Kimpen JL. Natural reinfection with respiratory syncytial virus does not boost virus-specific T-cell immunity. Pediatr Res 2002; 52:363-7; PMID:12193668; https://doi.org/10.1203/00006450-200209000-00009
   PubMed Web of Science ®Google Scholar
• Piedra PA. Clinical experience with respiratory syncytial virus vaccines. Pediatr Infect Dis J 2003; 22:S94-9; PMID:12671459
   PubMed Web of Science ®Google Scholar
• Leader S, Kohlhase K. Recent trends in severe respiratory syncytial virus (RSV) among US infants, 1997 to 2000. J Pediatr 2003; 143:S127-32; PMID:14615711; https://doi.org/10.1067/S0022-3476(03)00510-9
   PubMed Web of Science ®Google Scholar
• Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005; 352:1749-59; PMID:15858184; https://doi.org/10.1056/NEJMoa043951
   PubMed Web of Science ®Google Scholar
• Graham BS. Biological challenges and technological opportunities for respiratory syncytial virus vaccine development. Immunol Rev 2011; 239:149-66; PMID:21198670; https://doi.org/10.1111/j.1600-065X.2010.00972.x
   PubMed Web of Science ®Google Scholar
• Rudraraju R, Jones BG, Sealy R, Surman SL, Hurwitz JL. Respiratory syncytial virus: current progress in vaccine development. Viruses 2013; 5:577-94; PMID:23385470; https://doi.org/10.3390/v5020577
   PubMed Web of Science ®Google Scholar
• Afonso CL, Amarasinghe GK, Banyai K, Bao Y, Basler CF, Bavari S, Bejerman N, Blasdell KR, Briand FX, Briese T, et al. Taxonomy of the order Mononegavirales: update 2016. Arch Virol 2016; 161:2351-60; PMID:27216929; https://doi.org/10.1007/s00705-016-2880-1
   PubMed Web of Science ®Google Scholar
• Collins PL, Huang YT, Wertz GW. Identification of a tenth mRNA of respiratory syncytial virus and assignment of polypeptides to the 10 viral genes. J Virol 1984; 49:572-8; PMID:6546401
   PubMed Web of Science ®Google Scholar
• Levine S, Klaiber-Franco R, Paradiso PR. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol 1987; 68(Pt 9):2521-4; PMID:3655746; https://doi.org/10.1099/0022-1317-68-9-2521
   PubMed Web of Science ®Google Scholar
• Munoz FM, Piedra PA, Glezen WP. Safety and immunogenicity of respiratory syncytial virus purified fusion protein-2 vaccine in pregnant women. Vaccine 2003; 21:3465-7; PMID:12850361; https://doi.org/10.1016/S0264-410X(03)00352-9
   PubMed Web of Science ®Google Scholar
• Rey GU, Miao C, Caidi H, Trivedi SU, Harcourt JL, Tripp RA, Anderson LJ, Haynes LM. Decrease in formalin-inactivated respiratory syncytial virus (FI-RSV) enhanced disease with RSV G glycoprotein peptide immunization in BALB/c mice. PLoS One 2013; 8:e83075; PMID:24376637; https://doi.org/10.1371/journal.pone.0083075
   PubMed Web of Science ®Google Scholar
• Chin J, Magoffin RL, Shearer LA, Schieble JH, Lennette EH. Field evaluation of a respiratory syncytial virus vaccine and a trivalent parainfluenza virus vaccine in a pediatric population. Am J Epidemiol 1969; 89:449-63; PMID:4305200; https://doi.org/10.1093/oxfordjournals.aje.a120957
   PubMed Web of Science ®Google Scholar
• Karron RA, Buchholz UJ, Collins PL. Live-attenuated respiratory syncytial virus vaccines. Curr Top Microbiol Immunol 2013; 372:259-84; PMID:24362694
   PubMed Web of Science ®Google Scholar
• Lambert SL, Aslam S, Stillman E, MacPhail M, Nelson C, Ro B, Sweetwood R, Lei YM, Woo JC, Tang RS. A novel respiratory syncytial virus (RSV) F subunit vaccine adjuvanted with GLA-SE elicits robust protective TH1-type humoral and cellular immunity in rodent models. PLoS One 2015; 10:e0119509; PMID:25793508; https://doi.org/10.1371/journal.pone.0119509
   PubMed Web of Science ®Google Scholar
• Kim E, Okada K, Beeler JA, Crim RL, Piedra PA, Gilbert BE, Gambotto A. Development of an adenovirus-based respiratory syncytial virus vaccine: preclinical evaluation of efficacy, immunogenicity, and enhanced disease in a cotton rat model. J Virol 2014; 88:5100-8; PMID:24574396; https://doi.org/10.1128/JVI.03194-13
   PubMed Web of Science ®Google Scholar
• Moghaddam A, Olszewska W, Wang B, Tregoning JS, Helson R, Sattentau QJ, Openshaw PJ. A potential molecular mechanism for hypersensitivity caused by formalin-inactivated vaccines. Nat Med 2006; 12:905-7; PMID:16862151; https://doi.org/10.1038/nm1456
   PubMed Web of Science ®Google Scholar
• Murphy BR, Hall SL, Kulkarni AB, Crowe JE, Jr, Collins PL, Connors M, Karron RA, Chanock RM. An update on approaches to the development of respiratory syncytial virus (RSV) and parainfluenza virus type 3 (PIV3) vaccines. Virus Res 1994; 32:13-36; PMID:8030364; https://doi.org/10.1016/0168-1702(94)90059-0
   PubMed Web of Science ®Google Scholar
• Saade F, Petrovsky N. Technologies for enhanced efficacy of DNA vaccines. Expert Rev Vaccines 2012; 11:189-209; PMID:22309668; https://doi.org/10.1586/erv.11.188
   PubMed Web of Science ®Google Scholar
• Wahren B, Liu MA. DNA Vaccines: recent developments and the future. vaccines 2014; 2:785-96; https://doi.org/10.3390/vaccines2040785
   Google Scholar
• Ternette N, Stefanou D, Kuate S, Uberla K, Grunwald T. Expression of RNA virus proteins by RNA polymerase II dependent expression plasmids is hindered at multiple steps. Virol J 2007; 4:51; PMID:17550613; https://doi.org/10.1186/1743-422X-4-51
   PubMed Web of Science ®Google Scholar
• Stab V, Nitsche S, Niezold T, Storcksdieck Genannt Bonsmann M, Wiechers A, Tippler B, Hannaman D, Ehrhardt C, Uberla K, Grunwald T, et al. Protective efficacy and immunogenicity of a combinatory DNA vaccine against Influenza A Virus and the Respiratory Syncytial Virus. PLoS One 2013; 8:e72217; PMID:23967287; https://doi.org/10.1371/journal.pone.0072217
   PubMed Web of Science ®Google Scholar
• Hwang HS, Kwon YM, Lee JS, Yoo SE, Lee YN, Ko EJ, Kim MC, Cho MK, Lee YT, Jung YJ, et al. Co-immunization with virus-like particle and DNA vaccines induces protection against respiratory syncytial virus infection and bronchiolitis. Antiviral Res 2014; 110:115-23; PMID:25110201; https://doi.org/10.1016/j.antiviral.2014.07.016
   PubMed Web of Science ®Google Scholar
• Ko EJ, Kwon YM, Lee JS, Hwang HS, Yoo SE, Lee YN, Lee YT, Kim MC, Cho MK, Lee YR, et al. Virus-like nanoparticle and DNA vaccination confers protection against respiratory syncytial virus by modulating innate and adaptive immune cells. Nanomedicine 2015; 11:99-108; PMID:25109662
   PubMed Web of Science ®Google Scholar
• Hwang HS, Lee YT, Kim KH, Park S, Kwon YM, Lee Y, Ko EJ, Jung YJ, Lee JS, Kim YJ, et al. Combined virus-like particle and fusion protein-encoding DNA vaccination of cotton rats induces protection against respiratory syncytial virus without causing vaccine-enhanced disease. Virology 2016; 494:215-24; PMID:27123586; https://doi.org/10.1016/j.virol.2016.04.014
   PubMed Web of Science ®Google Scholar
• Wu H, Dennis VA, Pillai SR, Singh SR. RSV fusion (F) protein DNA vaccine provides partial protection against viral infection. Virus Res 2009; 145:39-47; PMID:19540885; https://doi.org/10.1016/j.virusres.2009.06.012
   PubMed Web of Science ®Google Scholar
• Klinman DM. Adjuvant activity of CpG oligodeoxynucleotides. Int Rev Immunol 2006; 25:135-54; PMID:16818369; https://doi.org/10.1080/08830180600743057
   PubMed Web of Science ®Google Scholar
• Barouch DH, Letvin NL, Seder RA. The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses. Immunol Rev 2004; 202:266-74; PMID:15546399; https://doi.org/10.1111/j.0105-2896.2004.00200.x
   PubMed Web of Science ®Google Scholar
• Groettrup M, Oehlschlaeger P. Prostate cancer dna vaccine. U.S. Patent 2013/0115239, issued May 9, 2013.
   Google Scholar
• Bembridge GP, Rodriguez N, Garcia-Beato R, Nicolson C, Melero JA, Taylor G. DNA encoding the attachment (G) or fusion (F) protein of respiratory syncytial virus induces protection in the absence of pulmonary inflammation. J Gen Virol 2000; 81:2519-23; PMID:10993942; https://doi.org/10.1099/0022-1317-81-10-2519
   PubMed Web of Science ®Google Scholar
• Ternette N, Tippler B, Uberla K, Grunwald T. Immunogenicity and efficacy of codon optimized DNA vaccines encoding the F-protein of respiratory syncytial virus. Vaccine 2007; 25:7271-9; PMID:17825960; https://doi.org/10.1016/j.vaccine.2007.07.025
   PubMed Web of Science ®Google Scholar
• Barnum SB SP, Vig K, Pillai S, Dennis VA, Singh SR. Nano-Encapsulated DNA and/or Protein Boost Immunizations Increase Efficiency of DNA Vaccine Protection against RSV. J Nanomedic Nanotechnol 2012; 3:132
   Google Scholar
• Taylor G, Bruce C, Barbet AF, Wyld SG, Thomas LH. DNA vaccination against respiratory syncytial virus in young calves. Vaccine 2005; 23:1242-50; PMID:15652666; https://doi.org/10.1016/j.vaccine.2004.09.005
   PubMed Web of Science ®Google Scholar
• Ohlschlager P, Spies E, Alvarez G, Quetting M, Groettrup M. The combination of TLR-9 adjuvantation and electroporation-mediated delivery enhances in vivo antitumor responses after vaccination with HPV-16 E7 encoding DNA. Int J Cancer 2011; 128:473-81; PMID:20309939; https://doi.org/10.1002/ijc.25344
   PubMed Web of Science ®Google Scholar
• Spies E, Reichardt W, Alvarez G, Groettrup M, Ohlschlager P. An artificial PAP gene breaks self-tolerance and promotes tumor regression in the TRAMP model for prostate carcinoma. Mol Ther 2012; 20:555-64; https://doi.org/10.1038/mt.2011.241
   Web of Science ®Google Scholar
• Lee S, Stokes KL, Currier MG, Sakamoto K, Lukacs NW, Celis E, Moore ML. Vaccine-elicited CD8+ T cells protect against respiratory syncytial virus strain A2-line19F-induced pathogenesis in BALB/c mice. J Virol 2012; 86:13016-24; PMID:23015695; https://doi.org/10.1128/JVI.01770-12
   PubMed Web of Science ®Google Scholar
• Coll RC, O'Neill LA. New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J Innate Immun 2010; 2:406-21; PMID:20505309; https://doi.org/10.1159/000315469
   PubMed Web of Science ®Google Scholar
• Tachibana R, Harashima H, Shinohara Y, Kiwada H. Quantitative studies on the nuclear transport of plasmid DNA and gene expression employing nonviral vectors. Adv Drug Deliv Rev 2001; 52:219-26; PMID:11718946; https://doi.org/10.1016/S0169-409X(01)00211-3
   PubMed Web of Science ®Google Scholar
• Li PP, Nakanishi A, Shum D, Sun PC, Salazar AM, Fernandez CF, Chan SW, Kasamatsu H. Simian virus 40 Vp1 DNA-binding domain is functionally separable from the overlapping nuclear localization signal and is required for effective virion formation and full viability. J Virol 2001; 75:7321-9; PMID:11462004; https://doi.org/10.1128/JVI.75.16.7321-7329.2001
   PubMed Web of Science ®Google Scholar
• Kim NY, Chang DS, Kim Y, Kim CH, Hur GH, Yang JM, Shin S. Enhanced Immune Response to DNA Vaccine Encoding Bacillus anthracis PA-D4 protects mice against Anthrax Spore challenge. PLoS One 2015; 10:e0139671; PMID:26430894; https://doi.org/10.1371/journal.pone.0139671
   PubMed Web of Science ®Google Scholar
• Costello HM, Ray WC, Chaiwatpongsakorn S, Peeples ME. Targeting RSV with vaccines and small molecule drugs. Infect Disord Drug Targets 2012; 12:110-28; PMID:22335496; https://doi.org/10.2174/187152612800100143
   PubMedGoogle Scholar
• Cobleigh MA, Wei X, Robek MD. A vesicular stomatitis virus-based therapeutic vaccine generates a functional CD8 T cell response to hepatitis B virus in transgenic mice. J Virol 2013; 87:2969-73; PMID:23269785; https://doi.org/10.1128/JVI.02111-12
   PubMed Web of Science ®Google Scholar
• Slon Campos JL, Poggianella M, Marchese S, Bestagno M, Burrone OR. Secretion of dengue virus envelope protein ectodomain from mammalian cells is dependent on domain II serotype and affects the immune response upon DNA vaccination. J Gen Virol 2015; 96:3265-79; PMID:26358704; https://doi.org/10.1099/jgv.0.000278
   PubMed Web of Science ®Google Scholar
• Kulkarni AB, Connors M, Firestone CY, Morse HC, 3rd, Murphy BR. The cytolytic activity of pulmonary CD8+ lymphocytes, induced by infection with a vaccinia virus recombinant expressing the M2 protein of respiratory syncytial virus (RSV), correlates with resistance to RSV infection in mice. J Virol 1993; 67:1044-9; PMID:8419638
   PubMed Web of Science ®Google Scholar
• Begona Ruiz-Arguello M, Gonzalez-Reyes L, Calder LJ, Palomo C, Martin D, Saiz MJ, García-Barreno B, Skehel JJ, Melero JA. Effect of proteolytic processing at two distinct sites on shape and aggregation of an anchorless fusion protein of human respiratory syncytial virus and fate of the intervening segment. Virology 2002; 298:317-26; PMID:12127793; https://doi.org/10.1006/viro.2002.1497
   PubMed Web of Science ®Google Scholar
• Krarup A, Truan D, Furmanova-Hollenstein P, Bogaert L, Bouchier P, Bisschop IJ, Widjojoatmodjo MN, Zahn R, Schuitemaker H, McLellan JS, et al. A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism. Nat Commun 2015; 6:8143; PMID:26333350; https://doi.org/10.1038/ncomms9143
   PubMed Web of Science ®Google Scholar
• McLellan JS, Yang Y, Graham BS, Kwong PD. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 2011; 85:7788-96; PMID:21613394; https://doi.org/10.1128/JVI.00555-11
   PubMed Web of Science ®Google Scholar
• Cimica V, Boigard H, Bhatia B, Fallon JT, Alimova A, Gottlieb P, Galarza JM. Novel Respiratory Syncytial Virus-Like Particle Vaccine Composed of the Postfusion and Prefusion Conformations of the F Glycoprotein. Clin Vaccine Immunol 2016; 23:451-9; PMID:27030590; https://doi.org/10.1128/CVI.00720-15
   PubMed Web of Science ®Google Scholar
• Lee JS, Kwon YM, Hwang HS, Lee YN, Ko EJ, Yoo SE, Kim MC, Kim KH, Cho MK, Lee YT, et al. Baculovirus-expressed virus-like particle vaccine in combination with DNA encoding the fusion protein confers protection against respiratory syncytial virus. Vaccine 2014; 32:5866-74; PMID:25173478; https://doi.org/10.1016/j.vaccine.2014.08.045
   PubMed Web of Science ®Google Scholar
• Chang J, Srikiatkhachorn A, Braciale TJ. Visualization and characterization of respiratory syncytial virus F-specific CD8(+) T cells during experimental virus infection. J Immunol 2001; 167:4254-60; PMID:11591747; https://doi.org/10.4049/jimmunol.167.8.4254
   PubMed Web of Science ®Google Scholar
• Farrag MA, Almajhdi FN. Human respiratory syncytial virus: Role of innate immunity in clearance and disease progression. Viral Immunol 2016; 29:11-26; PMID:26679242; https://doi.org/10.1089/vim.2015.0098
   PubMed Web of Science ®Google Scholar
• Schuurhof A, Bont L, Pennings JL, Hodemaekers HM, Wester PW, Buisman A, de Rond LC, Widjojoatmodjo MN, Luytjes W, Kimpen JL, et al. Gene expression differences in lungs of mice during secondary immune responses to respiratory syncytial virus infection. J Virol 2010; 84:9584-94; PMID:20592085; https://doi.org/10.1128/JVI.00302-10
   PubMed Web of Science ®Google Scholar
• Su YC, Townsend D, Herrero LJ, Zaid A, Rolph MS, Gahan ME, Nelson MA, Rudd PA, Matthaei KI, Foster PS, et al. Dual proinflammatory and antiviral properties of pulmonary eosinophils in respiratory syncytial virus vaccine-enhanced disease. J Virol 2015; 89:1564-78; PMID:25410867; https://doi.org/10.1128/JVI.01536-14
   PubMed Web of Science ®Google Scholar
• Dou Y, Zhao Y, Zhang ZY, Mao HW, Tu WW, Zhao XD. Respiratory syncytial virus infection induces higher Toll-like receptor-3 expression and TNF-alpha production than human metapneumovirus infection. PLoS One 2013; 8:e73488; PMID:24039959; https://doi.org/10.1371/journal.pone.0073488
   PubMed Web of Science ®Google Scholar
• Knudson CJ, Varga SM. The relationship between respiratory syncytial virus and asthma. Vet Pathol 2015; 52:97-106; PMID:24513802; https://doi.org/10.1177/0300985814520639
   PubMed Web of Science ®Google Scholar
• Lee YT, Kim KH, Hwang HS, Lee Y, Kwon YM, Ko EJ, Jung YJ, Lee YN, Kim MC, Kang SM. Innate and adaptive cellular phenotypes contributing to pulmonary disease in mice after respiratory syncytial virus immunization and infection. Virology 2015; 485:36-46; PMID:26196232; https://doi.org/10.1016/j.virol.2015.07.001
   PubMed Web of Science ®Google Scholar
• Schmidt MR, McGinnes LW, Kenward SA, Willems KN, Woodland RT, Morrison TG. Long-term and memory immune responses in mice against Newcastle disease virus-like particles containing respiratory syncytial virus glycoprotein ectodomains. J Virol 2012; 86:11654-62; PMID:22896618; https://doi.org/10.1128/JVI.01510-12
   PubMed Web of Science ®Google Scholar
• Ferraro B, Morrow MP, Hutnick NA, Shin TH, Lucke CE, Weiner DB. Clinical applications of DNA vaccines: current progress. Clin Infect Dis 2011; 53:296-302; PMID:21765081; https://doi.org/10.1093/cid/cir334
   PubMed Web of Science ®Google Scholar
• Wang R, Doolan DL, Le TP, Hedstrom RC, Coonan KM, Charoenvit Y, Jones TR, Hobart P, Margalith M, Ng J, et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 1998; 282:476-80; PMID:9774275; https://doi.org/10.1126/science.282.5388.476
   PubMed Web of Science ®Google Scholar
• Premenko-Lanier M, Rota PA, Rhodes GH, Bellini WJ, McChesney MB. Protection against challenge with measles virus (MV) in infant macaques by an MV DNA vaccine administered in the presence of neutralizing antibody. J Infect Dis 2004; 189:2064-71; PMID:15143474; https://doi.org/10.1086/420792
   PubMed Web of Science ®Google Scholar
• Hassett DE, Zhang J, Slifka M, Whitton JL. Immune responses following neonatal DNA vaccination are long-lived, abundant, and qualitatively similar to those induced by conventional immunization. J Virol 2000; 74:2620-7; PMID:10684276; https://doi.org/10.1128/JVI.74.6.2620-2627.2000
   PubMed Web of Science ®Google Scholar
• Almajhdi FN, Farrag MA, Amer HM. Genetic diversity in the G protein gene of group A human respiratory syncytial viruses circulating in Riyadh, Saudi Arabia. Arch Virol 2014; 159:73-81; PMID:23884633; https://doi.org/10.1007/s00705-013-1792-6
   PubMed Web of Science ®Google Scholar
• Gauger PC, Vincent AL. Serum virus neutralization assay for detection and quantitation of serum-neutralizing antibodies to influenza A virus in swine. Methods Mol Biol 2014; 1161:313-24; PMID:24899440
   PubMedGoogle Scholar
• Almajhdi FN, Senger T, Amer HM, Gissmann L, Ohlschlager P. Design of a highly effective therapeutic HPV16 E6/E7-specific DNA vaccine: optimization by different ways of sequence rearrangements (shuffling). PLoS One 2014; 9:e113461; PMID:25422946; https://doi.org/10.1371/journal.pone.0113461
   PubMed Web of Science ®Google Scholar
• Ohlschlager P, Pes M, Osen W, Durst M, Schneider A, Gissmann L, Kaufmann AM. An improved rearranged Human Papillomavirus Type 16 E7 DNA vaccine candidate (HPV-16 E7SH) induces an E7 wildtype-specific T cell response. Vaccine 2006; 24:2880-93; PMID:16472545; https://doi.org/10.1016/j.vaccine.2005.12.061
   PubMed Web of Science ®Google Scholar
• Murawski MR, McGinnes LW, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, Heaton PM, Fraire AE, Morrison TG. Newcastle disease virus-like particles containing respiratory syncytial virus G protein induced protection in BALB/c mice, with no evidence of immunopathology. J Virol 2010; 84:1110-23; PMID:19889768; https://doi.org/10.1128/JVI.01709-09
   PubMed Web of Science ®Google Scholar