Sublingual administration of a helper-dependent adenoviral vector expressing the codon-optimized soluble fusion glycoprotein of human respiratory syncytial virus elicits protective immunity in mice

Antiviral Research

Volumn 105, Issue 1, 2014, Pages 72-79

  Fu, Yuan Hui ^a   Jiao, Yue Ying ^a   He, Jin Sheng ^a   Giang, Gui Yuan ^c   Zhang, Wei ^d   Yan, Yi Fei ^a   Ma, Yao ^a   Hua, Ying ^a   Zhang, Ying ^a   Peng, Xiang Lei ^a   Shi, Chang Xin ^b   Hong, Tao ^a,e  

^a BEIJING JIAOTONG UNIVERSITY   (China)

^b MAYO CLINIC   (United States)

^c ANHUI MEDICAL UNIVERSITY   (China)

^d HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^e CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Human respiratory syncytial virus; Immune responses; Soluble fusion glycoprotein; Sublingual immunization

Indexed keywords

ADENOVIRUS VECTOR; GLYCOPROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN G ANTIBODY; SOLUBLE FUSION GLYCOPROTEIN; UNCLASSIFIED DRUG; DRUG CARRIER; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CODON; CONTROLLED STUDY; FEMALE; HUMORAL IMMUNITY; IN VITRO STUDY; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS PARTICLE; HELPER DEPENDENT ADENOVIRUS; INFECTION PREVENTION; SUBLINGUAL DRUG ADMINISTRATION; ADENOVIRIDAE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; DISEASE MODEL; GENETICS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; SERUM;

ADENOVIRIDAE; ADMINISTRATION, SUBLINGUAL; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; DRUG CARRIERS; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN G; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SERUM; VACCINES, SYNTHETIC;

EID: 84897857659     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2014.02.003     Document Type: Article

References (44)

1. D.M. Appledorn, Y.A. Aldhamen, S. Godbehere, S.S. Seregin, and A. Amalfitano Sublingual administration of an adenovirus serotype 5 (Ad5)-based vaccine confirms Toll-like receptor agonist activity in the oral cavity and elicits improved mucosal and systemic cell-mediated responses against HIV antigens despite preexisting Ad5 immunity Clin. Vaccine Immunol. 18 2011 150 160
2. I.M. Belyakov, B. Moss, W. Strober, and J.A. Berzofsky Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity Proc. Natl. Acad. Sci. U.S.A. 96 1999 4512 4517
3. J. Chang, A. Srikiatkhachorn, and T.J. Braciale Visualization and characterization of respiratory syncytial virus F-specific CD8(+) T cells during experimental virus infection J. Immunol. 167 2001 4254 4260
4. J.H. Choi, S.C. Schafer, L. Zhang, G.P. Kobinger, T. Juelich, A.N. Freiberg, and M.A. Croyle A single sublingual dose of an adenovirus-based vaccine protects against lethal Ebola challenge in mice and guinea pigs Mol. Pharm. 9 2012 156 167
5. P.L. Collins, and J.E. Crowe Respiratory syncytial virus and metapneumovirus D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus, Fields Virology 5th ed. 2007 Lippincott Williams & Wilkins Philadelphia 1601 1646
6. N. Cuburu, M.N. Kweon, J.H. Song, C. Hervouet, C. Luci, J.B. Sun, P. Hofman, J. Holmgren, F. Anjuere, and C. Czerkinsky Sublingual immunization induces broad-based systemic and mucosal immune responses in mice Vaccine 25 2007 8598 8610
7. R. Dahl, A. Kapp, G. Colombo, J.G. de Monchy, S. Rak, W. Emminger, B. Riis, P.M. Gronager, and S.R. Durham Sublingual grass allergen tablet immunotherapy provides sustained clinical benefit with progressive immunologic changes over 2 years J. Allergy Clin. Immunol. 121 512-518 2008 e512
8. R. Dahl, A. Kapp, G. Colombo, J.G. de Monchy, S. Rak, W. Emminger, M.F. Rivas, M. Ribel, and S.R. Durham Efficacy and safety of sublingual immunotherapy with grass allergen tablets for seasonal allergic rhinoconjunctivitis J. Allergy Clin. Immunol. 118 2006 434 440
9. D. Damjanovic, X. Zhang, J. Mu, M.F. Medina, and Z. Xing Organ distribution of transgene expression following intranasal mucosal delivery of recombinant replication-defective adenovirus gene transfer vector Genet. Vaccines Ther. 6 2008 5
10. A. Didier, H.J. Malling, M. Worm, F. Horak, S. Jager, A. Montagut, C. Andre, O. de Beaumont, and M. Melac Optimal dose, efficacy, and safety of once-daily sublingual immunotherapy with a 5-grass pollen tablet for seasonal allergic rhinitis J. Allergy Clin. Immunol. 120 2007 1338 1345
11. W. Domm, L. Brooks, H.L. Chung, C. Feng, W.J. Bowers, G. Watson, J.L. McGrath, and S. Dewhurst Robust antigen-specific humoral immune responses to sublingually delivered adenoviral vectors encoding HIV-1 Env: association with mucoadhesion and efficient penetration of the sublingual barrier Vaccine 29 2011 7080 7089
12. Y. Fu, J. He, X. Zheng, Q. Wu, M. Zhang, X. Wang, Y. Wang, C. Xie, Q. Tang, W. Wei, M. Wang, J. Song, J. Qu, Y. Zhang, and T. Hong Intranasal immunization with a replication-deficient adenoviral vector expressing the fusion glycoprotein of respiratory syncytial virus elicits protective immunity in BALB/c mice Biochem. Biophys. Res. Commun. 381 2009 528 532
13. Y.H. Fu, J.S. He, X.X. Zheng, X.B. Wang, C. Xie, C.X. Shi, M. Zhang, Q. Tang, W. Wei, J.G. Qu, and T. Hong Intranasal vaccination with a helper-dependent adenoviral vector enhances transgene-specific immune responses in BALB/c mice Biochem. Biophys. Res. Commun. 391 2010 857 861
14. Y.H. Fu, J.S. He, X.B. Wang, X.X. Zheng, Q. Wu, C. Xie, M. Zhang, W. Wei, Q. Tang, J.D. Song, J.G. Qu, and T. Hong A prime-boost vaccination strategy using attenuated Salmonella typhimurium and a replication-deficient recombinant adenovirus vector elicits protective immunity against human respiratory syncytial virus Biochem. Biophys. Res. Commun. 395 1 2010 87 92
15. B.S. Graham Biological challenges and technological opportunities for respiratory syncytial virus vaccine development Immunol. Rev. 239 2011 149 166
16. C.B. Hall Respiratory syncytial virus in young children Lancet 375 2010 1500 1502
17. C.B. Hall, G.A. Weinberg, M.K. Iwane, A.K. Blumkin, K.M. Edwards, M.A. Staat, P. Auinger, M.R. Griffin, K.A. Poehling, D. Erdman, C.G. Grijalva, Y. Zhu, and P. Szilagyi The burden of respiratory syncytial virus infection in young children N. Engl. J. Med. 360 2009 588 598
18. A. Harui, M.D. Roth, S.M. Kiertscher, K. Mitani, and S.K. Basak Vaccination with helper-dependent adenovirus enhances the generation of transgene-specific CTL Gene Ther. 11 2004 1617 1626
19. Z. Huo, S.L. Bissett, R. Giemza, S. Beddows, C. Oeser, and D.J. Lewis Systemic and mucosal immune responses to sublingual or intramuscular human papilloma virus antigens in healthy female volunteers PLoS One 7 2012 e33736
20. T.R. Johnson, D. Rangel, B.S. Graham, D.E. Brough, and J.G. Gall Genetic vaccine for respiratory syncytial virus provides protection without disease potentiation Mol. Ther. 22 2014 196 205
21. S. Jun, B. Clapp, D. Zlotkowska, T. Hoyt, K. Holderness, M. Maddaloni, and D.W. Pascual Sublingual immunization with adenovirus F protein-based vaccines stimulates protective immunity against botulinum neurotoxin A intoxication Int. Immunol. 24 2011 117 128
22. R.A. Karron Respiratory syncytial virus and parainfluenza virus vaccines S.A. Plotkin, W.A. Orenstein, P. Offit, Vaccines 5th ed. 2008 Saunders Elsevier Philadelphia 1283 1293
23. S. Kim, J.E. Jang, J.R. Yu, and J. Chang Single mucosal immunization of recombinant adenovirus-based vaccine expressing F1 protein fragment induces protective mucosal immunity against respiratory syncytial virus infection Vaccine 28 2010 3801 3808
24. R. Kohlmann, S. Schwannecke, B. Tippler, N. Ternette, V.V. Temchura, M. Tenbusch, K. Uberla, and T. Grunwald Protective efficacy and immunogenicity of an adenoviral vector vaccine encoding the codon-optimized F protein of respiratory syncytial virus J. Virol. 83 2009 12601 12610
25. F. Lemiale, W.P. Kong, L.M. Akyurek, X. Ling, Y. Huang, B.K. Chakrabarti, M. Eckhaus, and G.J. Nabel Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system J. Virol. 77 2003 10078 10087
26. V. Molinier-Frenkel, R. Lengagne, F. Gaden, S.S. Hong, J. Choppin, H. Gahery-Segard, P. Boulanger, and J.G. Guillet Adenovirus hexon protein is a potent adjuvant for activation of a cellular immune response J. Virol. 76 2002 127 135
27. V. Molinier-Frenkel, A. Prevost-Blondel, S.S. Hong, R. Lengagne, S. Boudaly, M.K. Magnusson, P. Boulanger, and J.G. Guillet The maturation of murine dendritic cells induced by human adenovirus is mediated by the fiber knob domain J. Biol. Chem. 278 2003 37175 37182
28. H. Nair, D.J. Nokes, B.D. Gessner, M. Dherani, S.A. Madhi, R.J. Singleton, K.L. O'Brien, A. Roca, P.F. Wright, N. Bruce, A. Chandran, E. Theodoratou, A. Sutanto, E.R. Sedyaningsih, M. Ngama, P.K. Munywoki, C. Kartasasmita, E.A. Simoes, I. Rudan, M.W. Weber, and H. Campbell Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis Lancet 375 2010 1545 1555
29. P. Ng, R.J. Parks, and F.L. Graham Preparation of helper-dependent adenoviral vectors Methods Mol. Med. 69 2002 371 388
30. N.J. Philpott, M. Nociari, K.B. Elkon, and E. Falck-Pedersen Adenovirus-induced maturation of dendritic cells through a PI3 kinase-mediated TNF-alpha induction pathway Proc. Natl. Acad. Sci. U.S.A. 101 2004 6200 6205
31. U.F. Power Respiratory syncytial virus (RSV) vaccines-two steps back for one leap forward J. Clin. Virol. 41 2008 38 44
32. S. Raghavan, A.K. Ostberg, C.F. Flach, A. Ekman, M. Blomquist, C. Czerkinsky, and J. Holmgren Sublingual immunization protects against Helicobacter pylori infection and induces T and B cell responses in the stomach Infect. Immun. 78 2010 4251 4260
33. M.D. Roth, Q. Cheng, A. Harui, S.K. Basak, K. Mitani, T.A. Low, and S.M. Kiertscher Helper-dependent adenoviral vectors efficiently express transgenes in human dendritic cells but still stimulate antiviral immune responses J. Immunol. 169 2002 4651 4656
34. H.Y. Shao, S.L. Yu, C. Sia, Y. Chen, E. Chitra, I.H. Chen, N. Venkatesan, C.H. Leng, P. Chong, and Y.H. Chow Immunogenic properties of RSV-B1 fusion (F) protein gene-encoding recombinant adenoviruses Vaccine 27 2009 5460 5471
35. B.S. Shim, K. Stadler, H.H. Nguyen, C.H. Yun, D.W. Kim, J. Chang, C. Czerkinsky, and M.K. Song Sublingual immunization with recombinant adenovirus encoding SARS-CoV spike protein induces systemic and mucosal immunity without redirection of the virus to the brain Virol. J. 9 2012 215
36. J.H. Song, J.I. Kim, H.J. Kwon, D.H. Shim, N. Parajuli, N. Cuburu, C. Czerkinsky, and M.N. Kweon CCR7-CCL19/CCL21-regulated dendritic cells are responsible for effectiveness of sublingual vaccination J. Immunol. 182 2009 6851 6860
37. J.H. Song, H.H. Nguyen, N. Cuburu, T. Horimoto, S.Y. Ko, S.H. Park, C. Czerkinsky, and M.N. Kweon Sublingual vaccination with influenza virus protects mice against lethal viral infection Proc. Natl. Acad. Sci. U.S.A. 105 2008 1644 1649
38. A. Srikiatkhachorn, and T.J. Braciale Virus-specific CD8+ T lymphocytes downregulate T helper cell type 2 cytokine secretion and pulmonary eosinophilia during experimental murine respiratory syncytial virus infection J. Exp. Med. 186 1997 421 432
39. X.B. Wang, J.S. He, Y.H. Fu, X.X. Zheng, and X. Fang Research on the methods for titrating respiratory syncytial virus Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 24 2010 147 149
40. E.A. Weaver, P.N. Nehete, S.S. Buchl, J.S. Senac, D. Palmer, P. Ng, K.J. Sastry, and M.A. Barry Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines PLoS One 4 2009 e5059
41. E.A. Weaver, P.N. Nehete, B.P. Nehete, S.J. Buchl, D. Palmer, D.C. Montefiori, P. Ng, K.J. Sastry, and M.A. Barry Protection against mucosal SHIV challenge by peptide and helper-dependent adenovirus vaccines Viruses 1 2009 920
42. T. Yamaguchi, K. Kawabata, N. Koizumi, F. Sakurai, K. Nakashima, H. Sakurai, T. Sasaki, N. Okada, K. Yamanishi, and H. Mizuguchi Role of MyD88 and TLR9 in the innate immune response elicited by serotype 5 adenoviral vectors Hum. Gene Ther. 18 2007 753 762
43. J.R. Yu, S. Kim, J.B. Lee, and J. Chang Single intranasal immunization with recombinant adenovirus-based vaccine induces protective immunity against respiratory syncytial virus infection J. Virol. 82 2008 2350 2357
44. T. Zhang, T. Hashizume, T. Kurita-Ochiai, and M. Yamamoto Sublingual vaccination with outer membrane protein of Porphyromonas gingivalis and Flt3 ligand elicits protective immunity in the oral cavity Biochem. Biophys. Res. Commun. 390 2009 937 941