Protection against respiratory syncytial virus by inactivated influenza virus carrying a fusion protein neutralizing epitope in a chimeric hemagglutinin

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 12, Issue 3, 2016, Pages 759-770

  Lee, Yu Na ^a   Hwang, Hye Suk ^a   Kim, Min Chul ^a,b   Lee, Young Tae ^a   Kim, Yu Jin ^a   Lee, F Eun Hyung ^c   Kang, Sang Moo ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Animal Plant and Fisheries Quarantine and Inspection Agency   (South Korea)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

F protein; Influenza virus; Neutralizing epitope vaccine; Recombinant; Respiratory syncytial virus; Viral vector

Indexed keywords

ANTIBODIES; CELLS; CYTOLOGY; FORMALDEHYDE; MAMMALS; PATHOLOGY; PROTEINS; RECOMBINANT PROTEINS; T-CELLS; VACCINES; VIRUSES;

INFLUENZA VIRUS; NEUTRALIZING EPITOPE; RECOMBINANT; RESPIRATORY SYNCYTIAL VIRUS; VIRAL VECTORS;

EPITOPES;

EPITOPE; FORMALDEHYDE; HEMAGGLUTININ; INTERLEUKIN 4; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS FUSION PROTEIN; INFLUENZA VACCINE; NEUTRALIZING ANTIBODY; RECOMBINANT PROTEIN; VIRUS HEMAGGLUTININ;

ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GENETIC ENGINEERING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNE RESPONSE; IMMUNIZATION; INFLUENZA VIRUS; MACROPHAGE; MOUSE; NONHUMAN; VIRUS INACTIVATION; VIRUS LOAD; VIRUS TITRATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; GENETICS; IMMUNOLOGY; ORTHOMYXOVIRIDAE; PROCEDURES; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELL LINE; EPITOPES; FEMALE; GENETIC ENGINEERING; HEMAGGLUTININS, VIRAL; HUMANS; IMMUNIZATION; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE; RECOMBINANT PROTEINS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUSES;

EID: 84959421945     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.11.007     Document Type: Article

References (60)

1. Falsey A.R., Hennessey P.A., Formica M.A., Cox C., Walsh E.E. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005, 352:1749-1759.
2. Nair H., Nokes D.J., Gessner B.D., Dherani M., Madhi S.A., Singleton R.J., 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.
3. Blanken M.O., Rovers M.M., Molenaar J.M., Winkler-Seinstra P.L., Meijer A., Kimpen J.L., et al. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N Engl J Med 2013, 368:1791-1799.
4. Kim H.W., Canchola J.G., Brandt C.D., Pyles G., Chanock R.M., Jensen K., et al. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 1969, 89:422-434.
5. Collins P.L., Graham B.S. Viral and host factors in human respiratory syncytial virus pathogenesis. J Virol 2008, 82:2040-2055.
6. Graham B.S. Biological challenges and technological opportunities for respiratory syncytial virus vaccine development. Immunol Rev 2011, 239:149-166.
7. Graham B.S., Anderson L.J. Challenges and opportunities for respiratory syncytial virus vaccines. Curr Top Microbiol Immunol 2013, 372:391-404.
8. Romero J.R. Palivizumab prophylaxis of respiratory syncytial virus disease from 1998 to 2002: results from four years of palivizumab usage. Pediatr Infect Dis J 2003, 22:S46-S54.
9. Johnson S., Oliver C., Prince G.A., Hemming V.G., Pfarr D.S., Wang S.C., 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.
10. Wu H., Pfarr D.S., Johnson S., Brewah Y.A., Woods R.M., Patel N.K., et al. Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J Mol Biol 2007, 368:652-665.
11. Andabaka T., Nickerson J.W., Rojas-Reyes M.X., Rueda J.D., Bacic Vrca V., Barsic B. Monoclonal antibody for reducing the risk of respiratory syncytial virus infection in children. Cochrane Database Syst Rev 2013, 4:CD006602.
12. Hoffmann E., Neumann G., Kawaoka Y., Hobom G., Webster R.G. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 2000, 97:6108-6113.
13. Garcia-Sastre A., Palese P. Influenza virus vectors. Biologicals 1995, 23:171-178.
14. Lee Y.N., Hwang H.S., Kim M.C., Lee Y.T., Lee J.S., Moore M.L., et al. Recombinant influenza virus expressing a fusion protein neutralizing epitope of respiratory syncytial virus (RSV) confers protection without vaccine-enhanced RSV disease. Antiviral Res 2015, 115:1-8.
15. Lee Y.N., Suk Hwang H., Kim M.C., Lee Y.T., Cho M.K., Kwon Y.M., et al. Recombinant influenza virus carrying the conserved domain of respiratory syncytial virus (RSV) G protein confers protection against RSV without inflammatory disease. Virology 2015, 476:217-225.
16. Li S., Polonis V., Isobe H., Zaghouani H., Guinea R., Moran T., et al. Chimeric influenza virus induces neutralizing antibodies and cytotoxic T cells against human immunodeficiency virus type 1. J Virol 1993, 67:6659-6666.
17. Li S.Q., Schulman J.L., Moran T., Bona C., Palese P. Influenza A virus transfectants with chimeric hemagglutinins containing epitopes from different subtypes. J Virol 1992, 66:399-404.
18. Hoffmann E., Krauss S., Perez D., Webby R., Webster R.G. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 2002, 20:3165-3170.
19. Prince G.A., Curtis S.J., Yim K.C., Porter D.D. Vaccine-enhanced respiratory syncytial virus disease in cotton rats following immunization with Lot 100 or a newly prepared reference vaccine. J Gen Virol 2001, 82:2881-2888.
20. Lee J.S., Kwon Y.M., Hwang H.S., Lee Y.N., Ko E.J., Yoo S.E., et al. Baculovirus-expressed virus-like particle vaccine in combination with DNA encoding the fusion protein confers protection against respiratory syncytial virus. Vaccine 2014, 32:5866-5874.
21. Anderson L.J., Bingham P., Hierholzer J.C. Neutralization of respiratory syncytial virus by individual and mixtures of F and G protein monoclonal antibodies. J Virol 1988, 62:4232-4238.
22. Ko E.J., Kwon Y.M., Lee J.S., Hwang H.S., Yoo S.E., Lee Y.N., 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.
23. Meyerholz D.K., Griffin M.A., Castilow E.M., Varga S.M. Comparison of histochemical methods for murine eosinophil detection in an RSV vaccine-enhanced inflammation model. Toxicol Pathol 2009, 37:249-255.
24. Hwang H.S., Kwon Y.M., Lee J.S., Yoo S.E., Lee Y.N., Ko E.J., et al. Co-immunization with virus-like particle and DNA vaccines induces protection against respiratory syncytial virus infection and bronchiolitis. Antiviral Res 2014, 110:115-123.
25. Murawski M.R., McGinnes L.W., Finberg R.W., Kurt-Jones E.A., Massare M.J., Smith G., et al. 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, 84:1110-1123.
26. Mok H., Lee S., Utley T.J., Shepherd B.E., Polosukhin V.V., Collier M.L., et al. Venezuelan equine encephalitis virus replicon particles encoding respiratory syncytial virus surface glycoproteins induce protective mucosal responses in mice and cotton rats. J Virol 2007, 81:13710-13722.
27. Caton A.J., Brownlee G.G., Yewdell J.W., Gerhard W. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982, 31:417-427.
28. Wiley D.C., Wilson I.A., Skehel J.J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981, 289:373-378.
29. McLellan J.S., Yang Y., Graham B.S., Kwong P.D. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 2011, 85:7788-7796.
30. Hawken J., Troy S.B. Adjuvants and inactivated polio vaccine: a systematic review. Vaccine 2012, 30:6971-6979.
31. Delgado M.F., Coviello S., Monsalvo A.C., Melendi G.A., Hernandez J.Z., Batalle J.P., 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.
32. Collins P.D., Marleau S., Griffiths-Johnson D.A., Jose P.J., Williams T.J. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med 1995, 182:1169-1174.
33. Castilow E.M., Meyerholz D.K., Varga S.M. IL-13 is required for eosinophil entry into the lung during respiratory syncytial virus vaccine-enhanced disease. J Immunol 2008, 180:2376-2384.
34. Johnson T.R., Rothenberg M.E., Graham B.S. Pulmonary eosinophilia requires interleukin-5, eotaxin-1, and CD4+ T cells in mice immunized with respiratory syncytial virus G glycoprotein. J Leukoc Biol 2008, 84:748-759.
35. Karlsson A.C., Martin J.N., Younger S.R., Bredt B.M., Epling L., Ronquillo R., et al. Comparison of the ELISPOT and cytokine flow cytometry assays for the enumeration of antigen-specific T cells. J Immunol Methods 2003, 283:141-153.
36. Chin J., Magoffin R.L., Shearer L.A., Schieble J.H., Lennette E.H. 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.
37. Ehlenfield D.R., Cameron K., Welliver R.C. Eosinophilia at the time of respiratory syncytial virus bronchiolitis predicts childhood reactive airway disease. Pediatrics 2000, 105:79-83.
38. Aherne W., Bird T., Court S.D., Gardner P.S., McQuillin J. Pathological changes in virus infections of the lower respiratory tract in children. J Clin Pathol 1970, 23:7-18.
39. Lugo R.A., Nahata M.C. Pathogenesis and treatment of bronchiolitis. Clin Pharm 1993, 12:95-116.
40. De Baets S., Schepens B., Sedeyn K., Schotsaert M., Roose K., Bogaert P., et al. Recombinant influenza virus carrying the respiratory syncytial virus (RSV) F85-93 CTL epitope reduces RSV replication in mice. J Virol 2013, 87:3314-3323.
41. Percy N., Barclay W.S., Garcia-Sastre A., Palese P. Expression of a foreign protein by influenza A virus. J Virol 1994, 68:4486-4492.
42. Bian C., Liu S., Liu N., Zhang G., Xing L., Song Y., et al. Influenza virus vaccine expressing fusion and attachment protein epitopes of respiratory syncytial virus induces protective antibodies in BALB/c mice. Antiviral Res 2014, 104:110-117.
43. Ferko B., Stasakova J., Sereinig S., Romanova J., Katinger D., Niebler B., et al. Hyperattenuated recombinant influenza A virus nonstructural-protein-encoding vectors induce human immunodeficiency virus type 1 Nef-specific systemic and mucosal immune responses in mice. J Virol 2001, 75:8899-8908.
44. Fonseca W., Ozawa M., Hatta M., Orozco E., Martinez M.B., Kawaoka Y. A recombinant influenza virus vaccine expressing the F protein of respiratory syncytial virus. Arch Virol 2013, 195:1067-1077.
45. Victor S.T., Watanabe S., Katsura H., Ozawa M., Kawaoka Y. A replication-incompetent PB2-knockout influenza A virus vaccine vector. J Virol 2012, 86:4123-4128.
46. Ohmit S.E., Petrie J.G., Cross R.T., Johnson E., Monto A.S. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccine-induced protection. J Infect Dis 2011, 204:1879-1885.
47. Cox R.J., Hovden A.O., Brokstad K.A., Szyszko E., Madhun A.S., Haaheim L.R. The humoral immune response and protective efficacy of vaccination with inactivated split and whole influenza virus vaccines in BALB/c mice. Vaccine 2006, 24:6585-6587.
48. Brett I.C., Johansson B.E. Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. Virology 2005, 339:273-280.
49. Kim Y.C., Quan F.S., Compans R.W., Kang S.M., Prausnitz M.R. Formulation and coating of microneedles with inactivated influenza virus to improve vaccine stability and immunogenicity. J Control Release 2010, 142:187-195.
50. Quan F.S., Kim Y.C., Yoo D.G., Compans R.W., Prausnitz M.R., Kang S.M. Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin. PLoS One 2009, 4.
51. Karron R.A., Wright P.F., Belshe R.B., Thumar B., Casey R., Newman F., et al. Identification of a recombinant live attenuated respiratory syncytial virus vaccine candidate that is highly attenuated in infants. J Infect Dis 2005, 191:1093-1104.
52. Wright P.F., Karron R.A., Madhi S.A., Treanor J.J., King J.C., O'Shea A., et al. The interferon antagonist NS2 protein of respiratory syncytial virus is an important virulence determinant for humans. J Infect Dis 2006, 193:573-581.
53. Murphy B.R., Sotnikov A.V., Lawrence L.A., Banks S.M., Prince G.A. Enhanced pulmonary histopathology is observed in cotton rats immunized with formalin-inactivated respiratory syncytial virus (RSV) or purified F glycoprotein and challenged with RSV 3-6 months after immunization. Vaccine 1990, 8:497-502.
54. Zhang P., Gu H., Bian C., Liu N., Li Z., Duan Y., et al. Characterization of recombinant influenza A virus as a vector expressing respiratory syncytial virus fusion protein epitopes. J Gen Virol 2014, 95:1886-1891.
55. General recommendations on immunization - recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2011, 60:1-64.
56. Castilow E.M., Varga S.M. Overcoming T cell-mediated immunopathology to achieve safe RSV vaccination. Future Virol 2008, 3:445-454.
57. Polack F.P., Teng M.N., Collins P.L., Prince G.A., Exner M., Regele H., et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J Exp Med 2002, 196:859-865.
58. Pribul P.K., Harker J., Wang B., Wang H., Tregoning J.S., Schwarze J., et al. Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J Virol 2008, 82:4441-4448.
59. Reed J.L., Brewah Y.A., Delaney T., Welliver T., Burwell T., Benjamin E., et al. Macrophage impairment underlies airway occlusion in primary respiratory syncytial virus bronchiolitis. J Infect Dis 2008, 198:1783-1793.
60. Shirey K.A., Lai W., Pletneva L.M., Karp C.L., Divanovic S., Blanco J.C., et al. Role of the lipoxygenase pathway in RSV-induced alternatively activated macrophages leading to resolution of lung pathology. Mucosal Immunol 2014, 7:549-557.