Single dose adenovirus vectored vaccine induces a potent and long-lasting immune response against rabbit hemorrhagic disease virus after parenteral or mucosal administration

Veterinary Immunology and Immunopathology

Volumn 142, Issue 3-4, 2011, Pages 179-188

  Fernández, Erlinda ^a   Toledo, Jorge R ^b   Chiong, Maylin ^a   Parra, Francisco ^c   Rodríguez, Elsa ^a   Montero, Carlos ^a   Méndez, Lídice ^a   Capucci, Lorenzo ^d   Farnós, Omar ^a  

^a CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

^c DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^d ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

Author keywords

Adenoviral vectors; Human Ad5; Rabbit hemorrhagic disease; Veterinary vaccination; VP60

Indexed keywords

ADENOVIRUS VECTOR; CAPSID PROTEIN; CUNIPRAVAC RHD; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; RABBIT HEMORRHAGIC DISEASE VIRUS VP60 CAPSID PROTEIN VACCINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS VACCINE; VP 60;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC IMMUNIZATION; HEMAGGLUTINATION INHIBITION TEST; HUMAN; HUMAN CELL; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PLASMID; PROTEIN EXPRESSION; RABBIT HEMORRHAGIC DISEASE; SALIVA ANALYSIS; SEROCONVERSION; SINGLE DRUG DOSE; VIRAL GENE DELIVERY SYSTEM; VIRUS STRAIN;

ADENOVIRIDAE; ADMINISTRATION, MUCOSAL; ANIMALS; ANTIBODIES, VIRAL; CALICIVIRIDAE INFECTIONS; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC VECTORS; HEMAGGLUTINATION INHIBITION TESTS; HEMORRHAGIC DISEASE VIRUS, RABBIT; IMMUNIZATION; MICE; MICE, INBRED BALB C; RABBITS; RANDOM ALLOCATION; STATISTICS, NONPARAMETRIC; VACCINES, SYNTHETIC; VIRAL STRUCTURAL PROTEINS; VIRAL VACCINES;

ADENOVIRIDAE; HEXAPODA; MIRIDAE; MUS; ORYCTOLAGUS CUNICULUS; RABBIT HEMORRHAGIC DISEASE VIRUS; REPLICATION COMPETENT VIRUSES;

EID: 79960049593     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2011.05.007     Document Type: Article

References (52)

1. Angulo E., Bárcena J. Towards a unique and transmissible vaccine against myxomatosis and rabbit haemorrhagic disease for rabbit populations. Wildl. Res. 2007, 34:567-577.
2. Babiuk L.A., Tikoo S.K. Adenoviruses as vectors for delivering vaccines to mucosal surfaces. J. Biotechnol. 2000, 83:105-113.
3. Bertagnoli S., Gelfi J., Le Gall G., Boilletot E., Vautherot J.F., Rasschaert D., Laurent S., Petit F., Boucrat-Baralon C., Milon A. Protection against myxomatosis and rabbit viral hemorrhagic disease with recombinant myxoma viruses expressing rabbit hemorrhagic disease virus capsid protein. J. Virol. 1996, 70:5061-5066.
4. Bertagnoli S., Gelfi J., Petit F., Vautherot J.F., Rasschaert D., Laurent S., Le Gall G., Boilletot E., Chantal J., Boucraut-Baralon C. Protection of rabbits against rabbit viral haemorrhagic disease with a vaccinia-RHDV recombinant virus. Vaccine 1996, 14:506-510.
5. Boga J.A., Martín-Alonso J.M., Casais R., Parra F. A single dose immunization with rabbit haemorrhagic disease virus major capsid protein produced in Saccharomyces cerevisiae induces protection. J. Gen. Virol. 1997, 78:2315-2318.
6. Bouslama A., De Mia G.M., Hammami S., Aouina T., Soussi H., Frescura T. Identification of the virus of rabbit haemorrhagic disease in Tunisia. Vet. Rec. 1996, 138:108-110.
7. Calvete C. Modeling the effect of population dynamics on the impact of rabbit hemorrhagic disease. Conserv. Biol. 2006, 20:1232-1241.
8. Capucci L., Fallacara F., Grazioli S., Lavazza A., Pacciarini M.L., Brocchi E. A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res. 1998, 58:115-126.
9. Capucci L., Frigoli G., Roenshold L., Lavazza A., Brocchi E., Rossi C. Antigenicity of the rabbit hemorrhagic disease virus studied by its reactivity with monoclonal antibodies. Virus Res. 1995, 37:221-238.
10. Casimiro D.R., Cox K., Tang A., Sykes K.J., Feng M., Wang F., Bett A., Schleif W.A., Liang X., Flynn J., Tobery T.W., Wilson K., Finnefrock A., Huang L., Vitelli S., Lin J., Patel D., Davies M.E., Heidecker G.J., Freed D.C., Dubey S., O'Connor D.H., Watkins D.I., Zhang Z.Q., Shiver J.W. Efficacy of multivalent adenovirus-based vaccine against simian immunodeficiency virus challenge. J. Virol. 2010, 84:2996-3003.
11. Castañón S., Marín M.S., Martín-Alonso J.M., Boga J.A., Casais R., Humara J.M., Ordás R.J., Parra F. Immunization with potato plants expressing VP60 protein protects against Rabbit Haemorrhagic Disease Virus. J. Virol. 1999, 73:4452-4455.
12. Chasey D. Rabbit haemorrhagic disease: the new scourge of Oryctolagus cuniculus. Lab. Anim. 1997, 31:33-44.
13. Cooke B.D., Robinson A.J., Merchant J.C., Nardin A., Capucci L. Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol. Infect. 2000, 124:563-576.
14. Cooke B.D. Rabbit haemorrhagic disease: field epidemiology and the management of wild rabbit populations. Rev. Sci. Tech. 2002, 21:347-358.
15. Dormond E., Perrier M., Kamen A. From the first to the third generation adenoviral vector: what parameters are governing the production yield?. Biotechnol. Adv. 2009, 27:133-144.
16. Farnós O., Boué O., Parra F., Martín-Alonso J.M., Joglar M., Valdés O., Navea L., Naranjo P., Lleonart R. High-level expression and immunogenic properties of the recombinant rabbit hemorrhagic disease virus VP60 capsid protein obtained in Pichia pastoris. J. Biotechnol. 2005, 117:215-224.
17. Farnós O., Fernández E., Chiong M., Parra F., Joglar M., Méndez L., Rodríguez E., Moya G., Rodríguez D., Lleonart R., González E.M., Alonso A., Alfonso P., Suárez M., Rodríguez M.P., Toledo J.R. Biochemical and structural characterization of RHDV capsid protein variants produced in Pichia pastoris: advantages for immunization strategies and vaccine implementation. Antivir. Res. 2009, 81:25-36.
18. Farnós O., Rodríguez D., Valdés O., Chiong M., Parra F., Toledo J.R., Fernández E., Lleonart R., Suárez M. Molecular and antigenic characterization of rabbit hemorrhagic disease virus isolated in Cuba indicates a distinct antigenic subtype. Arch. Virol. 2007, 152:1215-1221.
19. Fernández-Fernández M.R., Mourino M., Rivera J., Rodríguez F., Plana-Duran J., García J.A. Protection of rabbits against rabbit hemorrhagic disease virus by immunization with the VP60 protein expressed in plants with a potyvirus based vector. Virology 2001, 280:283-291.
20. Ferreira T.B., Alves P.M., Aunins J.G., Carrondo M.J.T. Use of adenoviral vectors as veterinary vaccines. Gene Ther. 2005, 12:73-83.
21. Fischer L., Le Gros F.X., Mason P.W., Paoletti E. A recombinant canarypox virus protects rabbits against a lethal rabbit hemorrhagic disease virus (RHDV) challenge. Vaccine 1997, 15:90-96.
22. Forrester N.L., Abubakr M.I., Abu Elzein E.M.E., al-Afaleq A.I., Housawi F.M.T., Moss S.R., Turner S.L., Gould E.A. Phylogenetic analysis of rabbit haemorrhagic disease virus strains from the Arabian Peninsula: did RHDV emerge simultaneously in Europe and Asia?. Virology 2006, 344:277-282.
23. Gogev S., Vanderheijden N., Lemaire M., Schynts F., D'Offay J., Deprez I., Adam M., Eloit M., Thiry E. Induction of protective immunity to bovine herpesvirus type 1 in cattle by intranasal administration of replication-defective human adenovirus type 5 expressing glycoprotein gC or gD. Vaccine 2002, 20:1451-1465.
24. He T.C., Zhou S., da Costa L.T., Yu J., Kinzle K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:2509-2514.
25. Higgins D.R., Cregg J.M. Introduction to Pichia pastoris. Pichia Protocols 1998, Humana Press Inc., Towota, pp. 1-15. R.D. Higgins, M.J. Cregg (Eds.).
26. Hoelscher M.A., Singh N., Garg S., Jayashankar L., Veguilla V., Pandey A., Matsuoka Y., Katz J.M., Donis R., Mittal S.K., Sambhara S. A broadly protective vaccine against globally dispersed clade 1 and clade 2 H5N1 influenza viruses. J. Infect. Dis. 2008, 197:1185-1188.
27. Hukowska-Szematowicz B., Pawlikowska M., Deptuła W. Genetic variability of Czech and German RHD virus strains. Pol. J. Microbiol. 2009, 58:237-245.
28. Kim S., Jang J.E., Yu J.R., Chang J. Single mucosal immunization of recombinant adenovirus-based vaccine expressing F1 protein fragment induces protective mucosal immunity against respiratory syncytial virus infection. Vaccine 2010, 28:3801-3808.
29. Laurent S., Vautherot J.F., Madelaine M.A., Le Gall G., Rasschaert D. Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into virus like particles and induces protection. J. Virol. 1994, 68:6794-6798.
30. Liu H., Liu X.M., Li Sh.Ch., Wu B.Ch., Ye L.L., Wang Q.W., Chen Z.L. A high-yield and scaleable adenovirus vector production process based on high density perfusion culture of HEK 293 cells as suspended aggregates. J. Biosci. Bioeng. 2009, 107:524-529.
31. Marchandeau S., Le Gall-Reculé G., Bertagnoli S., Aubineau J., Botti G., Lavazza A. Serological evidence for a non-protective RHDV-like virus. Vet. Res. 2005, 36:53-62.
32. Marín M.S., Martín-Alonso J.M., Pérez-Ordoyo García L.I., Argüello Villares J.L., Casais R., Venugopal K., Jiang W., Gould E.A., Parra F. Immunogenic properties of rabbit haemorrhagic disease virus structural protein VP60 expressed by a recombinant baculovirus: an efficient vaccine. Virus Res. 1995, 39:119-128.
33. McIntosh M.T., Behan S.C., Mohamed F.M., Lu Z., Moran K.E., Burrage T.G., Neilan J.G., Ward G.B., Botti G., Capucci L., Metwally S.A. A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virol. J. 2007, 4:96.
34. Meeusen E.N.T., Walker J., Peters A., Pastoret P.P., Jungersen G. Current status of veterinary vaccines. Clin. Microbiol. Rev. 2007, 20:489-510.
35. Meneses-Acosta A., Dormond E., Jacob D., Tom R., Bernier A., Perret S., St-Laurent G., Durocher Y., Gilbert R., Kamen A. Development of a suspension serum-free helper-dependent adenovirus production system and assessment of co-infection conditions. J. Virol. Methods 2008, 148:106-114.
36. Montesino R., Toledo J.R., Sánchez O., Sánchez A., Harvey D.J., Royle L., Dwek R.A., Rudd P.M., Gerwig G.J., Kamerling J.P., Cremata J.A. Monosialylated biantennary N-glycoforms containing GalNAc-GlcNAc antennae predominate when human EPO is expressed in goat milk. Arch. Biochem. Biophys. 2008, 470:163-175.
37. Oem J.K., Lee K.N., Roh I.S., Lee K.K., Kim S.H., Kim H.R., Park C.K., Joo Y.S. Identification and characterization of rabbit hemorrhagic disease virus genetic variants isolated in Korea. J. Vet. Med. Sci. 2009, 71:1519-1523.
38. O'Keefe J.S., Tempero J.E., Mothab M.X.J., Hansenb M.F., Atkinsona P.H. Serology of rabbit haemorrhagic disease virus in wild rabbits before and after release of the virus in New Zealand. Vet. Microbiol. 1999, 66:29-40.
39. Pacheco J.M., Brum M.C., Moraes M.P., Golde W.T., Grubman M.J. Rapid protection of cattle from direct challenge with foot-and-mouth disease virus (FMDV) by a single inoculation with an adenovirus-vectored FMDV subunit vaccine. Virology 2005, 337:205-209.
40. Parra F., Prieto M. Purification of a calicivirus as the causative agent of a lethal hemorrhagic disease in rabbits. J. Virol. 1990, 64:4013-4015.
41. Peiperl L., Morgan C., Moodie Z., Li H., Russell N., Graham B.S., Tomaras G.D., De Rosa S.C., McElrath M.J. Safety and immunogenicity of a replication-defective adenovirus type 5 HIV vaccine in Ad5-seronegative persons: a randomized clinical trial (HVTN 054). PLoS ONE 2010, 5:e13579.
42. Pérez-Filgueira D.M., Resino-Talaván P., Cubillos C., Angulo I., Barderas M.G., Bárcena J., Escribano J.M. Development of a low-cost, insect larvae-derived recombinant subunit vaccine against RHDV. Virology 2007, 364:422-430.
43. Sánchez O., Montesino R., Toledo J.R., Rodríguez E., Díaz D., Royle L., Rudd P.M., Dwek R.A., Gerwig G.J., Kamerling J.P., Harvey D.J., Cremata J.A. The goat mammary glandular epithelial (GMGE) cell line promotes polyfucosylation and N,N′-diacetyllactosediaminylation of N-glycans linked to recombinant human erythropoietin. Arch. Biochem. Biophys. 2007, 464:322-334.
44. Sánchez O., González A., Gómez-Puerta S., Noda J., Vega A., Águila J.C., Suárez L., Parra N.C., Toledo J.R. Avian CD154 enhances humoral and cellular immune responses induced by an adenovirus vector-based vaccine in chickens. Comp. Immunol. Microbiol. Infectious Dis. 2010, 28:7907-7914.
45. Santuosso M., McCormick S., Zhang X., Zganiacz A., Xing Z. Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect. Immun. 2006, 74:4634-4643.
46. Schirrmeier H., Reimann I., Kollner B., Granzow H. Pathogenic, antigenic and molecular properties of rabbit haemorrhagic disease virus (RHDV) isolated from vaccinated rabbits: detection and characterization of antigenic variants. Arch. Virol. 1999, 144:719-735.
47. Sun Y., Liu D.F., Wang Y.F., Liang B.B., Cheng D., Li N., Qi Q.F., Zhu Q.H., Qiu H.J. Generation and efficacy evaluation of a recombinant adenovirus expressing the E2 protein of classical swine fever virus. Res. Vet. Sci. 2010, 88:77-82.
48. Suzuki M., Cela R., Clarke C., Bertin T.K., Mouriño S., Lee B. Large-scale production of high-quality helper-dependent adenoviral vectors using adherent cells in cell factories. Hum. Gene Ther. 2010, 21:120-126.
49. Toledo J.R., Sánchez O., Montesino R., García G., Montañez M., Zamora P.A., Rodríguez M.P., Cremata J.A. High expression level of recombinant human erythropoietin in the milk of non-transgenic goats. J. Biotechnol. 2006, 123:225-235.
50. Toledo J.R., Sánchez O., Montesino R., Farnos O., Rodríguez M.P., Alfonso P., Oramas N., Rodríguez E., Santana E., Vega E., Ganges L., Frias M.T., Cremata J., Barrera M. Highly protective E2-CSFV vaccine candidate produced in the mammary gland of adenoviral transduced goats. J. Biotechnol. 2008, 133:370-376.
51. Tucker S.N., Tingley D.W., Scallan C.D. Oral adenoviral-based vaccines: historical perspective and future opportunity. Expert Rev. Vaccines 2008, 7:25-31.
52. Wesley R.D., Lager K.M. Evaluation of a recombinant human adenovirus-5 vaccine administered via needle-free device and intramuscular injection for vaccination of pigs against swine influenza virus. Am. J. Vet. Res. 2005, 66:1943-1947.