A new rabies vaccine based on a recombinant Orf virus (Parapoxvirus) expressing the rabies virus glycoprotein

Journal of Virology

Volumn 87, Issue 3, 2013, Pages 1618-1630

  Amann, Ralf ^a,d   Rohde, Jörg ^a,d   Wulle, Ulrich ^a,d   Conlee, Douglas ^b   Raue, Rudiger ^c   Martinon, Olivier ^b   Rziha, Hanns Joachim ^a,d  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b ZOETIS   (United States)

^c PFIZER INC   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

D1701 V RABG VACCINE; NEUTRALIZING ANTIBODY; RABIES VACCINE; RABIES VIRUS GLYCOPROTEIN; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CAT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOG; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POXVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABIES; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; VACCINATION; VIRUS IMMUNITY; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CATS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; DOGS; DRUG CARRIERS; FEMALE; GENETIC VECTORS; GLYCOPROTEINS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; ORF VIRUS; RABIES; RABIES VACCINES; RABIES VIRUS; SURVIVAL ANALYSIS; VIRAL ENVELOPE PROTEINS;

EID: 84873034067     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02470-12     Document Type: Article

References (71)

1. Lembo T, Hampson K, Kaare MT, Ernest E, Knobel D, Kazwala RR, Haydon DT, Cleaveland S. 2010. The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Negl. Trop. Dis. 4:e626.
2. Dietzschold B, Schnell M, Koprowski H. 2005. Pathogenesis of rabies. Curr. Top. Microbiol. Immunol. 292:45-56.
3. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A. 2010. The cell biology of rabies virus: using stealth to reach the brain. Nat. Rev. Microbiol. 8:51-61.
4. Cox JH, Dietzschold B, Schneider LG. 1977. Rabies virus glycoprotein. II. Biological and serological characterization. Infect. Immun. 16:754-759.
5. Foley HD, McGettigan JP, Siler CA, Dietzschold B, Schnell MJ. 2000. A recombinant rabies virus expressing vesicular stomatitis virus glycoprotein fails to protect against rabies virus infection. Proc. Natl. Acad. Sci. U. S. A. 97:14680-14685.
6. Macfarlan RI, Dietzschold B, Koprowski H. 1986. Stimulation of cytotoxic T-lymphocyte responses by rabies virus glycoprotein and identification of an immunodominant domain. Mol. Immunol. 23:733-741.
7. Wiktor TJ, Gyorgy E, Schlumberger D, Sokol F, Koprowski H. 1973. Antigenic properties of rabies virus components. J. Immunol. 110:269-276.
8. Moore SM, Wilkerson MJ, Davis RD, Wyatt CR, Briggs DJ. 2006. Detection of cellular immunity to rabies antigens in human vaccinees. J. Clin. Immunol. 26:533-545.
9. Aubert MF, Masson E, Artois M, Barrat J. 1994. Oral wildlife rabies vaccination field trials in Europe, with recent emphasis on France. Curr. Top. Microbiol. Immunol. 187:219-243.
10. Rupprecht CE, Wiktor TJ, Johnston DH, Hamir AN, Dietzschold B, Wunner WH, Glickman LT, Koprowski H. 1986. Oral immunization and protection of raccoons (Procyon lotor) with a vaccinia-rabies glycoprotein recombinant virus vaccine. Proc. Natl. Acad. Sci. U. S. A. 83:7947-7950.
11. Rupprecht CE, Hanlon CA, Blanton J, Manangan J, Morrill P, Murphy S, Niezgoda M, Orciari LA, Schumacher CL, Dietzschold B. 2005. Oral vaccination of dogs with recombinant rabies virus vaccines. Virus Res. 111:101-105.
12. Conzelmann KK, Schnell M. 1994. Rescue of synthetic genomic RNA analogs of rabies virus by plasmid-encoded proteins. J. Virol. 68:713-719.
13. Gomme EA, Wanjalla CN, Wirblich C, Schnell MJ. 2011. Rabies virus as a research tool and viral vaccine vector. Adv. Virus Res. 79:139-164.
14. Ertl HC. 2009. Novel vaccines to human rabies. PLoS Negl Trop. Dis. 3:e515.
15. Cenna J, Hunter M, Tan GS, Papaneri AB, Ribka EP, Schnell MJ, Marx PA, McGettigan JP. 2009. Replication-deficient rabies virus-based vaccines are safe and immunogenic in mice and nonhuman primates. J. Infect. Dis. 200:1251-1260.
16. Faber M, Li J, Kean RB, Hooper DC, Alugupalli KR, Dietzschold B. 2009. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc. Natl. Acad. Sci. U. S. A. 106:11300-11305.
17. Wen Y, Wang H, Wu H, Yang F, Tripp RA, Hogan RJ, Fu ZF. 2011. Rabies virus expressing dendritic cell-activating molecules enhances the innate and adaptive immune response to vaccination. J. Virol. 85:1634-1644.
18. Zhao L, Toriumi H, Wang H, Kuang Y, Guo X, Morimoto K, Fu ZF. 2010. Expression of MIP-1alpha (CCL3) by a recombinant rabies virus enhances its immunogenicity by inducing innate immunity and recruiting dendritic cells and B cells. J. Virol. 84:9642-9648.
19. Ullas PT. 2012. Rabies DNA vaccines: current status and future. World J. Vaccines 2:36-45.
20. Kaur M, Saxena A, Rai A, Bhatnagar R. 2010. Rabies DNA vaccine encoding lysosome-targeted glycoprotein supplemented with Emulsigen- D confers complete protection in preexposure and postexposure studies in BALB/c mice. FASEB J. 24:173-183.
21. Liu MA. 2011. DNA vaccines: an historical perspective and view to the future. Immunol. Rev. 239:62-84.
22. Ge J, Wang X, Tao L, Wen Z, Feng N, Yang S, Xia X, Yang C, Chen H, Bu Z. 2011. Newcastle disease virus-vectored rabies vaccine is safe, highly immunogenic, and provides long-lasting protection in dogs and cats. J. Virol. 85:8241-8252.
23. Saxena S, Dahiya SS, Sonwane AA, Patel CL, Saini M, Rai A, Gupta PK. 2008. A sindbis virus replicon-based DNA vaccine encoding the rabies virus glycoprotein elicits immune responses and complete protection in mice from lethal challenge. Vaccine 26:6592-6601.
24. Yuan Z, Zhang S, Liu Y, Zhang F, Fooks AR, Li Q, Hu R. 2008. A recombinant pseudorabies virus expressing rabies virus glycoprotein: safety and immunogenicity in dogs. Vaccine 26:1314-1321.
25. Prehaud C, Takehara K, Flamand A, Bishop DH. 1989. Immunogenic and protective properties of rabies virus glycoprotein expressed by baculovirus vectors. Virology 173:390-399.
26. Weyer J, Rupprecht CE, Nel LH. 2009. Poxvirus-vectored vaccines for rabies-a review. Vaccine 27:7198-7201.
27. Kieny MP, Lathe R, Drillien R, Spehner D, Skory S, Schmitt D, Wiktor T, Koprowski H, Lecocq JP. 1984. Expression of rabies virus glycoprotein from a recombinant vaccinia virus. Nature 312:163-166.
28. Wiktor TJ, Macfarlan RI, Reagan KJ, Dietzschold B, Curtis PJ, Wunner WH, Kieny MP, Lathe R, Lecocq JP, Mackett M, et al. 1984. Protection from rabies by a vaccinia virus recombinant containing the rabies virus glycoprotein gene. Proc. Natl. Acad. Sci. U. S. A. 81:7194-7198.
29. Blancou J, Kieny MP, Lathe R, Lecocq JP, Pastoret PP, Soulebot JP, Desmettre P. 1986. Oral vaccination of the fox against rabies using a live recombinant vaccinia virus. Nature 322:373-375.
30. Rupprecht CE, Charlton KM, Artois M, Casey GA, Webster WA, Campbell JB, Lawson KF, Schneider LG. 1990. Ineffectiveness and comparative pathogenicity of attenuated rabies virus vaccines for the striped skunk (Mephitis mephitis). J. Wildl. Dis. 26:99-102.
31. Rupprecht CE, Blass L, Smith K, Orciari LA, Niezgoda M, Whitfield SG, Gibbons RV, Guerra M, Hanlon CA. 2001. Human infection due to recombinant vaccinia-rabies glycoprotein virus. N. Engl. J. Med. 345:582-586.
32. Lodmell DL, Ewalt LC. 2000. Rabies vaccination: comparison of neutralizing antibody responses after priming and boosting with different combinations of DNA, inactivated virus, or recombinant vaccinia virus vaccines. Vaccine 18:2394-2398.
33. Weyer J, Rupprecht CE, Mans J, Viljoen GJ, Nel LH. 2007. Generation and evaluation of a recombinant modified vaccinia virus Ankara vaccine for rabies. Vaccine 25:4213-4222.
34. Esposito JJ, Knight JC, Shaddock JH, Novembre FJ, Baer GM. 1988. Successful oral rabies vaccination of raccoons with raccoon poxvirus recombinants expressing rabies virus glycoprotein. Virology 165:313-316.
35. Taylor J, Trimarchi C, Weinberg R, Languet B, Guillemin F, Desmettre P, Paoletti E. 1991. Efficacy studies on a canarypox-rabies recombinant virus. Vaccine 9:190-193.
36. Taylor J, Weinberg R, Languet B, Desmettre P, Paoletti E. 1988. Recombinant fowlpox virus inducing protective immunity in non-avian species. Vaccine 6:497-503.
37. Aspden K, van Dijk AA, Bingham J, Cox D, Passmore JA, Williamson AL. 2002. Immunogenicity of a recombinant lumpy skin disease virus (neethling vaccine strain) expressing the rabies virus glycoprotein in cattle. Vaccine 20:2693-2701.
38. Büttner M, Rziha H-J. 2002. Parapoxviruses: from the lesion to the viral genome. J. Vet. Med. B Infect. Dis. Vet. Public Health 49:7-16.
39. Hussain KA, Burger D. 1989. In vivo and in vitro characteristics of contagious ecthyma virus isolates: host response mechanism. Vet. Microbiol. 19:23-36.
40. Haig DM. 2006. Orf virus infection and host immunity. Curr. Opin. Infect. Dis. 19:127-131.
41. Fachinger V, Schlapp T, Strube W, Schmeer N, Saalmuller A. 2000. Poxvirus-induced immunostimulating effects on porcine leukocytes. J. Virol. 74:7943-7951.
42. Friebe A, Siegling A, Friederichs S, Volk HD, Weber O. 2004. Immunomodulatory effects of inactivated parapoxvirus ovis (ORF virus) on human peripheral immune cells: induction of cytokine secretion in monocytes and Th1-like cells. J. Virol. 78:9400-9411.
43. Siegemund S, Hartl A, H von Buttlar Dautel F, Raue R, Freudenberg MA, Fejer G, Buttner M, Kohler G, Kirschning CJ, Sparwasser T, Alber G. 2009. Conventional bone marrow-derived dendritic cells contribute to Toll-like receptor-independent production of alpha/beta interferon in response to inactivated parapoxvirus ovis. J. Virol. 83:9411-9422.
44. Fischer T, Planz O, Stitz L, Rziha H-J. 2003. Novel recombinant parapoxvirus vectors induce protective humoral and cellular immunity against lethal herpesvirus challenge infection in mice. J. Virol. 77:9312-9323.
45. Friebe A, Friederichs S, Scholz K, Janssen U, Scholz C, Schlapp T, Mercer A, Siegling A, Volk HD, Weber O. 2011. Characterization of immunostimulatory components of Orf virus (parapoxvirus ovis). J. Gen. Virol. 92:1571-1584.
46. McGuire MJ, Johnston SA, Sykes KF. 2012. Novel immune-modulator identified by a rapid, functional screen of the parapoxvirus ovis (Orf virus) genome. Proteome Sci. 10:4.
47. Weber O, Siegling A, Friebe A, Limmer A, Schlapp T, Knolle P, Mercer A, Schaller H, Volk HD. 2003. Inactivated parapoxvirus ovis (Orf virus) has antiviral activity against hepatitis B virus and herpes simplex virus. J. Gen. Virol. 84:1843-1852.
48. Rziha H-J, Henkel M, Cottone R, Bauer B, Auge U, Gotz F, Pfaff E, Rottgen M, Dehio C, Büttner M. 2000. Generation of recombinant parapoxviruses: nonessential genes suitable for insertion and expression of foreign genes. J. Biotechnol. 83:137-145.
49. Rohde J, Schirrmeier H, Granzow H, Rziha H-J. 2011. A new recombinant Orf virus (ORFV, parapoxvirus) protects rabbits against lethal infection with rabbit hemorrhagic disease virus (RHDV). Vaccine 29:9256-9264.
50. Voigt H, Merant C, Wienhold D, Braun A, Hutet E, Le Potier MF, Saalmuller A, Pfaff E, Büttner M. 2007. Efficient priming against classical swine fever with a safe glycoprotein E2 expressing Orf virus recombinant (ORFV VrV-E2). Vaccine 25:5915-5926.
51. Henkel M, Planz O, Fischer T, Stitz L, Rziha H-J. 2005. Prevention of virus persistence and protection against immunopathology after Borna disease virus infection of the brain by a novel Orf virus recombinant. J. Virol. 79:314-325.
52. Dory D, Fischer T, Beven V, Cariolet R, Rziha H-J, Jestin A. 2006. Prime-boost immunization using DNA vaccine and recombinant Orf virus protects pigs against pseudorabies virus (herpes suid 1). Vaccine 24: 6256-6263.
53. van Rooij EM, Rijsewijk FA, Moonen-Leusen HW, Bianchi AT, Rziha H-J. 2010. Comparison of different prime-boost regimes with DNA and recombinant Orf virus based vaccines expressing glycoprotein D of pseudorabies virus in pigs. Vaccine 28:1808-1813.
54. Klingen Y, Conzelmann KK, Finke S. 2008. Double-labeled rabies virus: live tracking of enveloped virus transport. J. Virol. 82:237-245.
55. Cobbold SP, Jayasuriya A, Nash A, Prospero TD, Waldmann H. 1984. Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo. Nature 312:548-551.
56. Le Gros GS, Prestidge RL, Watson JD. 1983. In-vivo modulation of thymus-derived lymphocytes with monoclonal antibodies in mice. I. Effect of anti-Thy-1 antibody on the tissue distribution of lymphocytes. Immunology 50:537-546.
57. Brun A, Albina E, Barret T, Chapman DA, Czub M, Dixon LK, Keil GM, Klonjkowski B, Le Potier MF, Libeau G, Ortego J, Richardson J, Takamatsu HH. 2008. Antigen delivery systems for veterinary vaccine development. Viral-vector based delivery systems. Vaccine 26:6508-6528.
58. Li J, Faber M, Papaneri A, Faber ML, McGettigan JP, Schnell MJ, Dietzschold B. 2006. A single immunization with a recombinant canine adenovirus expressing the rabies virusGprotein confers protective immunity against rabies in mice. Virology 356:147-154.
59. Dietzschold B, Tollis M, Rupprecht CE, Celis E, Koprowski H. 1987. Antigenic variation in rabies and rabies-related viruses: cross-protection independent of glycoprotein-mediated virus-neutralizing antibody. J. Infect. Dis. 156:815-822.
60. Gulati U, Kumari K, Wu W, Keitel WA, Air GM. 2005. Amount and avidity of serum antibodies against native glycoproteins and denatured virus after repeated influenza whole-virus vaccination. Vaccine 23:1414-1425.
61. Kanesa-thasan N, Smucny JJ, Hoke CH, Marks DH, Konishi E, Kurane I, Tang DB, Vaughn DW, Mason PW, Shope RE. 2000. Safety and immunogenicity of NYVAC-JEV and ALVAC-JEV attenuated recombinant Japanese encephalitis virus-poxvirus vaccines in vaccinianonimmune and vaccinia-immune humans. Vaccine 19:483-491.
62. Kundig TM, Kalberer CP, Hengartner H, Zinkernagel RM. 1993. Vaccination with two different vaccinia recombinant viruses: long-term inhibition of secondary vaccination. Vaccine 11:1154-1158.
63. McCoy K, Tatsis N, Korioth-Schmitz B, Lasaro MO, Hensley SE, Lin SW, Li Y, Giles-Davis W, Cun A, Zhou D, Xiang Z, Letvin NL, Ertl HC. 2007. Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J. Virol. 81:6594-6604.
64. Sharpe S, Polyanskaya N, Dennis M, Sutter G, Hanke T, Erfle V, Hirsch V, Cranage M. 2001. Induction of simian immunodeficiency virus (SIV)- specific CTL in rhesus macaques by vaccination with modified vaccinia virus Ankara expressing SIV transgenes: influence of pre-existing antivector immunity. J. Gen. Virol. 82:2215-2223.
65. Whitmire JK. 2011. Induction and function of virus-specific CD4+T cell responses. Virology 411:216-228.
66. Swain SL, McKinstry KK, Strutt TM. 2012. Expanding roles for CD4(+) T cells in immunity to viruses. Nat. Rev. Immunol. 12:136-148.
67. Perry LL, Lodmell DL. 1991. Role of CD4+ and CD8+ T cells in murine resistance to street rabies virus. J. Virol. 65:3429-3434.
68. Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B. 1998. Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J. Virol. 72:3711-3719.
69. Gherardi MM, Esteban M. 2005. Recombinant poxviruses as mucosal vaccine vectors. J. Gen. Virol. 86:2925-2936.
70. Minke JM, Bouvet J, Cliquet F, Wasniewski M, Guiot AL, Lemaitre L, Cariou C, Cozette V, Vergne L, Guigal PM. 2009. Comparison of antibody responses after vaccination with two inactivated rabies vaccines. Vet. Microbiol. 133:283-286.
71. Hu R, Zhang S, Fooks AR, Yuan H, Liu Y, Li H, Tu C, Xia X, Xiao Y. 2006. Prevention of rabies virus infection in dogs by a recombinant canine adenovirus type-2 encoding the rabies virus glycoprotein. Microbes Infect. 8:1090-1097.