Mucosal delivery of a vectored RSV vaccine is safe and elicits protective immunity in rodents and nonhuman primates

Molecular Therapy Methods and Clinical Development

Volumn 2, Issue , 2015, Pages 15018-

  Pierantoni, Angiolo ^a   Esposito, Maria Luisa ^a   Ammendola, Virginia ^a   Napolitano, Federico ^a   Grazioli, Fabiana ^a   Abbate, Adele ^a   del Sorbo, Mariarosaria ^a   Siani, Loredana ^a   D'Alise, Anna Morena ^a   Taglioni, Alessandra ^c   Perretta, Gemma ^c   Siccardi, Antonio ^d   Soprana, Elisa ^d   Panigada, Maddalena ^d   Thom, Michelle ^b   Scarselli, Elisa ^a   Folgori, Antonella ^a   Colloca, Stefano ^a   Taylor, Geraldine ^b   Cortese, Riccardo ^a,g   Nicosia, Alfredo ^a,e,f   Capone, Stefania ^a   Vitelli, Alessandra ^a   more..

^a ReiThera Srl ^*  (Italy)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c CNR   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^g Keires AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; F PROTEIN; IMMUNOGLOBULIN A; NEUTRALIZING ANTIBODY; RESPIRATORY SYNCYTIAL VIRUS VACCINE; UNCLASSIFIED DRUG; VIRAL PROTEIN; B LYMPHOCYTE ANTIGEN; GUANINE NUCLEOTIDE BINDING PROTEIN; M2 1 PROTEIN; T LYMPHOCYTE ANTIGEN;

ADENOVIRIDAE; ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; COTTON RAT; DRUG POTENCY; DRUG SAFETY; FEMALE; HELA CELL LINE; HETEROLOGOUS IMMUNITY; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; LOWER RESPIRATORY TRACT INFECTION; LUNG; MOUSE; MUCOSAL DRUG ADMINISTRATION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RAT; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RODENT; VACCINIA VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRUS IMMUNITY; VIRUS REPLICATION; ANIMAL CELL; ANIMAL MODEL; ANTIGEN EXPRESSION; CELL LYSATE; DOSE RESPONSE; DRUG EFFICACY; EMBRYO; FOOT AND MOUTH DISEASE VIRUS; LIMIT OF DETECTION; MACACA FASCICULARIS; MOLECULAR WEIGHT; MUCOSAL IMMUNITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; T LYMPHOCYTE; VACCINATION; WESTERN BLOTTING;

EID: 85015169841     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2015.18     Document Type: Article

References (50)

1. 1 Nair, H, Simões, EA, Rudan, I, Gessner, BD, Azziz-Baumgartner, E, Zhang, JS, et al., Severe Acute Lower Respiratory Infections Working Group. Global and regional burden of hospital admissions for severe acute lower respiratory infections in young children in 2010: a systematic analysis. Lancet 381 (2013), 1380–1390.
2. 2 Falsey, AR, Editorial commentary: respiratory syncytial virus: a global pathogen in an aging world. Clin Infect Dis 57 (2013), 1078–1080.
3. 3 The IMpact-RSV Study Group. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. Pediatrics 102 (1998), 531–537.
4. 4 Fulginiti, VA, Eller, JJ, Sieber, OF, Joyner, JW, Minamitani, M, Meiklejohn, G, 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 89 (1969), 435–448.
5. 5 Kapikian, AZ, Mitchell, RH, Chanock, RM, Shvedoff, RA, Stewart, CE, 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 89 (1969), 405–421.
6. 6 Connors, M, Giese, NA, Kulkarni, AB, Firestone, CY, Morse, HC 3rd, Murphy, BR, Enhanced pulmonary histopathology induced by respiratory syncytial virus (RSV) challenge of formalin-inactivated RSV-immunized BALB/c mice is abrogated by depletion of interleukin-4 (IL-4) and IL-10. J Virol 68 (1994), 5321–5325.
7. 7 Polack, FP, Teng, MN, Collins, PL, Prince, GA, Exner, M, Regele, H, et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J Exp Med 196 (2002), 859–865.
8. 8 Groothuis, JR, Simoes, EA, Levin, MJ, Hall, CB, Long, CE, Rodriguez, WJ, et al. Prophylactic administration of respiratory syncytial virus immune globulin to high-risk infants and young children. The Respiratory Syncytial Virus Immune Globulin Study Group. N Engl J Med 329 (1993), 1524–1530.
9. 9 Hussell, T, Baldwin, CJ, O'Garra, A, Openshaw, PJ, CD8+ T cells control Th2-driven pathology during pulmonary respiratory syncytial virus infection. Eur J Immunol 27 (1997), 3341–3349.
10. 10 Walsh, EE, Falsey, AR, Humoral and mucosal immunity in protection from natural respiratory syncytial virus infection in adults. J Infect Dis 190 (2004), 373–378.
11. 11 Cherukuri, A, Patton, K, Gasser, RA Jr, Zuo, F, Woo, J, Esser, MT, et al. Adults 65 years old and older have reduced numbers of functional memory T cells to respiratory syncytial virus fusion protein. Clin Vaccine Immunol 20 (2013), 239–247.
12. 12 de Bree, GJ, Heidema, J, van Leeuwen, EM, van Bleek, GM, Jonkers, RE, Jansen, HM, et al. Respiratory syncytial virus-specific CD8+ memory T cell responses in elderly persons. J Infect Dis 191 (2005), 1710–1718.
13. 13 Liniger, M, Zuniga, A, Naim, HY, Use of viral vectors for the development of vaccines. Expert Rev Vaccines 6 (2007), 255–266.
14. 14 Fu, Y, He, J, Zheng, X, Wu, Q, Zhang, M, Wang, X, et al. 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.
15. 15 Kohlmann, R, Schwannecke, S, Tippler, B, Ternette, N, Temchura, VV, Tenbusch, M, et al. 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.
16. 16 Kim, E, Okada, K, Beeler, JA, Crim, RL, Piedra, PA, Gilbert, BE, et al. Development of an adenovirus-based respiratory syncytial virus vaccine: preclinical evaluation of efficacy, immunogenicity, and enhanced disease in a cotton rat model. J Virol 88 (2014), 5100–5108.
17. 17 Johnson, TR, Rangel, D, Graham, BS, Brough, DE, Gall, JG, Genetic vaccine for respiratory syncytial virus provides protection without disease potentiation. Mol Ther 22 (2014), 196–205.
18. 18 Anderson, R, Huang, Y, Langley, JM, Prospects for defined epitope vaccines for respiratory syncytial virus. Future Microbiol 5 (2010), 585–602.
19. 19 Vitelli, A, Quirion, MR, Lo, CY, Misplon, JA, Grabowska, AK, Pierantoni, A, et al. Vaccination to conserved influenza antigens in mice using a novel Simian adenovirus vector, PanAd3, derived from the bonobo Pan paniscus. PLoS One, 8, 2013, e55435.
20. 20 Piedra, PA, Jewell, AM, Cron, SG, Atmar, RL, Glezen, WP, Correlates of immunity to respiratory syncytial virus (RSV) associated-hospitalization: establishment of minimum protective threshold levels of serum neutralizing antibodies. Vaccine 21 (2003), 3479–3482.
21. 21 Fang, J, Qian, JJ, Yi, S, Harding, TC, Tu, GH, VanRoey, M, et al. Stable antibody expression at therapeutic levels using the 2A peptide. Nat Biotechnol 23 (2005), 584–590.
22. 22 Taylor, G, Stott, EJ, Furze, J, Ford, J, Sopp, P, Protective epitopes on the fusion protein of respiratory syncytial virus recognized by murine and bovine monoclonal antibodies. J Gen Virol 73(Pt 9) (1992), 2217–2223.
23. 23 Woodland, DL, Intranasal vaccination. Viral Immunol, 26, 2013, 125.
24. 24 Boukhvalova, MS, Blanco, JC, The cotton rat Sigmodon hispidus model of respiratory syncytial virus infection. Curr Top Microbiol Immunol 372 (2013), 347–358.
25. 25 Gerdts, V, Littel-van den Hurk, Sv, Griebel, PJ, Babiuk, LA, Use of animal models in the development of human vaccines. Future Microbiol 2 (2007), 667–675.
26. 26 Brand, P, Häussinger, K, Meyer, T, Scheuch, G, Schulz, H, Selzer, T, et al. Intrapulmonary distribution of deposited particles. J Aerosol Med 12 (1999), 275–284.
27. 27 Chaiwatpongsakorn, S, Epand, RF, Collins, PL, Epand, RM, Peeples, ME, Soluble respiratory syncytial virus fusion protein in the fully cleaved, pretriggered state is triggered by exposure to low-molarity buffer. J Virol 85 (2011), 3968–3977.
28. 28 McLellan, JS, Chen, M, Leung, S, Graepel, KW, Du, X, Yang, Y, et al. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340 (2013), 1113–1117.
29. 29 Smith, G, Raghunandan, R, Wu, Y, Liu, Y, Massare, M, Nathan, M, et al. Respiratory syncytial virus fusion glycoprotein expressed in insect cells form protein nanoparticles that induce protective immunity in cotton rats. PLoS One, 7, 2012, e50852.
30. 30 Swanson, KA, Settembre, EC, Shaw, CA, Dey, AK, Rappuoli, R, Mandl, CW, 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 108 (2011), 9619–9624.
31. 31 Prince, GA, Horswood, RL, Chanock, RM, Quantitative aspects of passive immunity to respiratory syncytial virus infection in infant cotton rats. J Virol 55 (1985), 517–520.
32. 32 Larrañaga, CL, Ampuero, SL, Luchsinger, VF, Carrión, FA, Aguilar, NV, Morales, PR, et al. Impaired immune response in severe human lower tract respiratory infection by respiratory syncytial virus. Pediatr Infect Dis J 28 (2009), 867–873.
33. 33 Fishaut, M, Tubergen, D, McIntosh, K, Cellular response to respiratory viruses with particular reference to children with disorders of cell-mediated immunity. J Pediatr 96 (1980), 179–186.
34. 34 Hall, CB, Powell, KR, MacDonald, NE, Gala, CL, Menegus, ME, Suffin, SC, et al. Respiratory syncytial viral infection in children with compromised immune function. N Engl J Med 315 (1986), 77–81.
35. 35 Lee, FE, Walsh, EE, Falsey, AR, Liu, N, Liu, D, Divekar, A, et al. The balance between influenza- and RSV-specific CD4 T cells secreting IL-10 or IFNgamma in young and healthy-elderly subjects. Mech Ageing Dev 126 (2005), 1223–1229.
36. 36 Olson, MR, Varga, SM, CD8 T cells inhibit respiratory syncytial virus (RSV) vaccine-enhanced disease. J Immunol 179 (2007), 5415–5424.
37. 37 Cannon, MJ, Openshaw, PJ, Askonas, BA, Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J Exp Med 168 (1988), 1163–1168.
38. 38 Vallbracht, S, Jessen, B, Mrusek, S, Enders, A, Collins, PL, Ehl, S, et al. Influence of a single viral epitope on T cell response and disease after infection of mice with respiratory syncytial virus. J Immunol 179 (2007), 8264–8273.
39. 39 Capone, S, D'Alise, AM, Ammendola, V, Colloca, S, Cortese, R, Nicosia, A, et al. Development of chimpanzee adenoviruses as vaccine vectors: challenges and successes emerging from clinical trials. Expert Rev Vaccines 12 (2013), 379–393.
40. 40 Edgar, RC, MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 2004, 113.
41. 41 Waterhouse, AM, Procter, JB, Martin, DM, Clamp, M, Barton, GJ, Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 (2009), 1189–1191.
42. 42 Graham, FL, Smiley, J, Russell, WC, Nairn, R, Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36 (1977), 59–74.
43. 43 Matthews, DA, Cummings, D, Evelegh, C, Graham, FL, Prevec, L, Development and use of a 293 cell line expressing lac repressor for the rescue of recombinant adenoviruses expressing high levels of rabies virus glycoprotein. J Gen Virol 80 (Pt 2) (1999), 345–353.
44. 44 Evans, RK, Nawrocki, DK, Isopi, LA, Williams, DM, Casimiro, DR, Chin, S, et al. Development of stable liquid formulations for adenovirus-based vaccines. J Pharm Sci 93 (2004), 2458–2475.
45. 45 Di Lullo, G, Soprana, E, Panigada, M, Palini, A, Agresti, A, Comunian, C, et al. The combination of marker gene swapping and fluorescence-activated cell sorting improves the efficiency of recombinant modified vaccinia virus Ankara vaccine production for human use. J Virol Methods 163 (2010), 195–204.
46. 46 Di Lullo, G, Soprana, E, Panigada, M, Palini, A, Erfle, V, Staib, C, et al. Marker gene swapping facilitates recombinant Modified Vaccinia Virus Ankara production by host-range selection. J Virol Methods 156 (2009), 37–43.
47. 47 Capone, S, Naddeo, M, D'Alise, AM, Abbate, A, Grazioli, F, Del Gaudio, A, et al. Fusion of HCV nonstructural antigen to MHC class II-associated invariant chain enhances T-cell responses induced by vectored vaccines in nonhuman primates. Mol Ther 22 (2014), 1039–1047.
48. 48 Taylor, G, Stott, EJ, Hughes, M, Collins, AP, Respiratory syncytial virus infection in mice. Infect Immun 43 (1984), 649–655.
49. 49 Hallak, LK, Spillmann, D, Collins, PL, Peeples, ME, Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol 74 (2000), 10508–10513.
50. 50 Chen, M, Chang, JS, Nason, M, Rangel, D, Gall, JG, Graham, BS, et al. A flow cytometry-based assay to assess RSV-specific neutralizing antibody is reproducible, efficient and accurate. J Immunol Methods 362 (2010), 180–184.