Recombinant Rabies Viruses Expressing GM-CSF or Flagellin Are Effective Vaccines for Both Intramuscular and Oral Immunizations

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Zhou, Ming ^a,b,c   Zhang, Guoqing ^b   Ren, Guiping ^b   Gnanadurai, Clement W ^b   Li, Zhenguang ^b   Chai, Qingqing ^b   Yang, Yang ^b   Leyson, Christina M ^b   Wu, Wenxue ^c   Cui, Min ^a   Fu, Zhen F ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF GEORGIA   (United States)

^c CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; RABIES VACCINE; RECOMBINANT RABIES VIRUS LBNSE EXPRESSING FLAGELLIN; RECOMBINANT RABIES VIRUS LBNSE EXPRESSING GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VACCINE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFICACY; DRUG SCREENING; FEMALE; HAMSTER; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; LD 50; MOLECULAR CLONING; MOUSE; NONHUMAN; RABIES; VACCINATION; VIRUS GENOME; VIRUS VIRULENCE;

ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CELL LINE; CRICETINAE; DENDRITIC CELLS; FEMALE; FLAGELLIN; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INJECTIONS, INTRAMUSCULAR; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE, INBRED BALB C; MICE, INBRED ICR; RABIES; RABIES VIRUS; VACCINATION; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 84877913776     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063384     Document Type: Article

References (73)

1. Fu ZF, (1997) Rabies and rabies research: past, present and future. Vaccine 15Suppl: S20-24.
2. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, et al. (2005) Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83: 360-368.
3. Rupprecht CE, Smith JS, Fekadu M, Childs JE, (1995) The ascension of wildlife rabies: a cause for public health concern or intervention? Emerg Infect Dis 1: 107-114.
4. Nigg AJ, Walker PL, (2009) Overview, prevention, and treatment of rabies. Pharmacotherapy 29: 1182-1195.
5. Morimoto K, Patel M, Corisdeo S, Hooper DC, Fu ZF, et al. (1996) Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. Proc Natl Acad Sci U S A 93: 5653-5658.
6. Centers for Disease C, Prevention (2012) U.s-acquired human rabies with symptom onset and diagnosis abroad, 2012. MMWR Morb Mortal Wkly Rep 61: 777-781.
7. Wu X, Smith TG, Rupprecht CE, (2011) From brain passage to cell adaptation: the road of human rabies vaccine development. Expert Rev Vaccines 10: 1597-1608.
8. Aghomo HO, Oduye OO, Rupprecht CE, (1990) The serological response of young dogs to the Flury LEP strain of rabies virus vaccine. Vet Res Commun 14: 415-425.
9. Clark KA, Wilson PJ, (1996) Postexposure rabies prophylaxis and preexposure rabies vaccination failure in domestic animals. J Am Vet Med Assoc 208: 1827-1830.
10. Estrada R, Vos A, De Leon R, Mueller T, (2001) Field trial with oral vaccination of dogs against rabies in the Philippines. BMC Infect Dis 1: 23.
11. Schneider LG, Cox JH, Muller WW, Hohnsbeen KP, (1988) Current oral rabies vaccination in Europe: an interim balance. Rev Infect Dis 10Suppl 4: S654-659.
12. Wandeler AI, Capt S, Kappeler A, Hauser R, (1988) Oral immunization of wildlife against rabies: concept and first field experiments. Rev Infect Dis 10Suppl 4: S649-653.
13. Winkler WG, Shaddock JH, Williams LW, (1976) Oral rabies vaccine: evaluation of its infectivity in three species of rodents. Am J Epidemiol 104: 294-298.
14. Esh JB, Cunningham JG, Wiktor TJ, (1982) Vaccine-induced rabies in four cats. J Am Vet Med Assoc 180: 1336-1339.
15. Lafay F, Benejean J, Tuffereau C, Flamand A, Coulon P, (1994) Vaccination against rabies: construction and characterization of SAG2, a double avirulent derivative of SADBern. Vaccine 12: 317-320.
16. Flamand A, Coulon P, Lafay F, Tuffereau C, (1993) Avirulent mutants of rabies virus and their use as live vaccine. Trends Microbiol 1: 317-320.
17. Cliquet F, Robardet E, Must K, Laine M, Peik K, et al. (2012) Eliminating rabies in Estonia. PLoS Negl Trop Dis 6: e1535.
18. Cliquet F, Aubert M, (2004) Elimination of terrestrial rabies in Western European countries. Dev Biol (Basel) 119: 185-204.
19. Niin E, Barrat J, Kristian M, Demerson JM, Cliquet F, (2006) First oral vaccination of wildlife against rabies in Estonia. Dev Biol (Basel) 125: 145-147.
20. Hanlon CA, Niezgoda M, Morrill P, Rupprecht CE, (2002) Oral efficacy of an attenuated rabies virus vaccine in skunks and raccoons. J Wildl Dis 38: 420-427.
21. Kieny MP, Lathe R, Drillien R, Spehner D, Skory S, et al. (1984) Expression of rabies virus glycoprotein from a recombinant vaccinia virus. Nature 312: 163-166.
22. Brochier B, Kieny MP, Costy F, Coppens P, Bauduin B, et al. (1991) Large-scale eradication of rabies using recombinant vaccinia-rabies vaccine. Nature 354: 520-522.
23. Fearneyhough MG, Wilson PJ, Clark KA, Smith DR, Johnston DH, et al. (1998) Results of an oral rabies vaccination program for coyotes. J Am Vet Med Assoc 212: 498-502.
24. Hanlon CA, Niezgoda M, Hamir AN, Schumacher C, Koprowski H, et al. (1998) First North American field release of a vaccinia-rabies glycoprotein recombinant virus. J Wildl Dis 34: 228-239.
25. Robbins AH, Borden MD, Windmiller BS, Niezgoda M, Marcus LC, et al. (1998) Prevention of the spread of rabies to wildlife by oral vaccination of raccoons in Massachusetts. J Am Vet Med Assoc 213: 1407-1412.
26. Roscoe DE, Holste WC, Sorhage FE, Campbell C, Niezgoda M, et al. (1998) Efficacy of an oral vaccinia-rabies glycoprotein recombinant vaccine in controlling epidemic raccoon rabies in New Jersey. J Wildl Dis 34: 752-763.
27. Mempel M, Isa G, Klugbauer N, Meyer H, Wildi G, et al. (2003) Laboratory acquired infection with recombinant vaccinia virus containing an immunomodulating construct. J Invest Dermatol 120: 356-358.
28. Rupprecht CE, Blass L, Smith K, Orciari LA, Niezgoda M, et al. (2001) Human infection due to recombinant vaccinia-rabies glycoprotein virus. N Engl J Med 345: 582-586.
29. Centers for Disease Control and Prevention (2009) Human vaccinia infection after contact with a raccoon rabies vaccine bait- Pennsylvania, 2009. MMWR Morb Mortal Wkly Rep 58: 1204-1207.
30. Wen Y, Wang H, Wu H, Yang F, Tripp RA, et al. (2011) Rabies virus expressing dendritic cell-activating molecules enhances the innate and adaptive immune response to vaccination. J Virol 85: 1634-1644.
31. Lee F, Yokota T, Otsuka T, Gemmell L, Larson N, et al. (1985) Isolation of cDNA for a human granulocyte-macrophage colony-stimulating factor by functional expression in mammalian cells. Proc Natl Acad Sci U S A 82: 4360-4364.
32. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD, (2003) The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170: 5165-5175.
33. Pino O, Martin M, Michalek SM, (2005) Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica serovar typhimurium to potentiate mucosal and systemic responses. Infection and Immunity 73: 6763-6770.
34. Didierlaurent A, Ferrero I, Otten LA, Dubois B, Reinhardt M, et al. (2004) Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172: 6922-6930.
35. Tsujimoto H, Uchida T, Efron PA, Scumpia PO, Verma A, et al. (2005) Flagellin enhances NK cell proliferation and activation directly and through dendritic cell-NK cell interactions. J Leukoc Biol 78: 888-897.
36. McEwen J, Levi R, Horwitz RJ, Arnon R, (1992) Synthetic recombinant vaccine expressing influenza haemagglutinin epitope in Salmonella flagellin leads to partial protection in mice. Vaccine 10: 405-411.
37. Levi R, Arnon R, (1996) Synthetic recombinant influenza vaccine induces efficient long-term immunity and cross-strain protection. Vaccine 14: 85-92.
38. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT, (2002) Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J Immunol 169: 3914-3919.
39. Honko AN, Sriranganathan N, Lees CJ, Mizel SB, (2006) Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74: 1113-1120.
40. Pino O, Martin M, Michalek SM, (2005) Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect Immun 73: 6763-6770.
41. Bates JT, Honko AN, Graff AH, Kock ND, Mizel SB, (2008) Mucosal adjuvant activity of flagellin in aged mice. Mech Ageing Dev 129: 271-281.
42. Lee SE, Kim SY, Jeong BC, Kim YR, Bae SJ, et al. (2006) A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect Immun 74: 694-702.
43. Mizel SB, Graff AH, Sriranganathan N, Ervin S, Lees CJ, et al. (2009) Flagellin-F1-V Fusion Protein Is an Effective Plague Vaccine in Mice and Two Species of Nonhuman Primates. Clinical and Vaccine Immunology 16: 21-28.
44. Rasalingam P, Rossiter JP, Mebatsion T, Jackson AC, (2005) Comparative pathogenesis of the SAD-L16 strain of rabies virus and a mutant modifying the dynein light chain binding site of the rabies virus phosphoprotein in young mice. Virus Res 111: 55-60.
45. Conzelmann KK, Cox JH, Schneider LG, Thiel HJ, (1990) Molecular cloning and complete nucleotide sequence of the attenuated rabies virus SAD B19. Virology 175: 485-499.
46. Faber M, Faber ML, Li J, Preuss MA, Schnell MJ, et al. (2007) Dominance of a nonpathogenic glycoprotein gene over a pathogenic glycoprotein gene in rabies virus. J Virol 81: 7041-7047.
47. Schnell MJ, Mebatsion T, Conzelmann KK, (1994) Infectious rabies viruses from cloned cDNA. EMBO J 13: 4195-4203.
48. Reed LJ, H Muench, (1938) A simple method of estimating fifty percent end points. Am J Hyg 27: 493-497.
49. Gilboa E, (2007) DC-based cancer vaccines. J Clin Invest 117: 1195-1203.
50. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
51. Zhao L, Toriumi H, Wang H, Kuang Y, Guo X, et al. (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.
52. Inoue K, Shoji Y, Kurane I, Iijima T, Sakai T, et al. (2003) An improved method for recovering rabies virus from cloned cDNA. J Virol Methods 107: 229-236.
53. Agrawal S, Agrawal A, Doughty B, Gerwitz A, Blenis J, et al. (2003) Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J Immunol 171: 4984-4989.
54. Mizel SB, Graff AH, Sriranganathan N, Ervin S, Lees CJ, et al. (2009) Flagellin-F1-V fusion protein is an effective plague vaccine in mice and two species of nonhuman primates. Clin Vaccine Immunol 16: 21-28.
55. Ahmed M, Puckett S, Arimilli S, Braxton CL, Mizel SB, et al. (2010) Stimulation of human dendritic cells by wild-type and M protein mutant vesicular stomatitis viruses engineered to express bacterial flagellin. J Virol 84: 12093-12098.
56. McDonald WF, Huleatt JW, Foellmer HG, Hewitt D, Tang J, et al. (2007) A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 195: 1607-1617.
57. Delaney KN, Phipps JP, Johnson JB, Mizel SB, (2010) A recombinant flagellin-poxvirus fusion protein vaccine elicits complement-dependent protection against respiratory challenge with vaccinia virus in mice. Viral Immunol 23: 201-210.
58. Liu G, Song L, Reiserova L, Trivedi U, Li H, et al. (2012) Flagellin-HA vaccines protect ferrets and mice against H5N1 highly pathogenic avian influenza virus (HPAIV) infections. Vaccine 30: 6833-6838.
59. Meslin FX, Fishbein DB, Matter HC, (1994) Rationale and prospects for rabies elimination in developing countries. Curr Top Microbiol Immunol 187: 1-26.
60. Charlton KM, Artois M, Prevec L, Campbell JB, Casey GA, et al. (1992) Oral rabies vaccination of skunks and foxes with a recombinant human adenovirus vaccine. Arch Virol 123: 169-179.
61. Stohr K, Meslin FM, (1996) Progress and setbacks in the oral immunisation of foxes against rabies in Europe. Vet Rec 139: 32-35.
62. MacInnes CD, Smith SM, Tinline RR, Ayers NR, Bachmann P, et al. (2001) Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis 37: 119-132.
63. Vos A, Neubert A, Pommerening E, Muller T, Dohner L, et al. (2001) Immunogenicity of an E1-deleted recombinant human adenovirus against rabies by different routes of administration. J Gen Virol 82: 2191-2197.
64. Li J, Faber M, Papaneri A, Faber ML, McGettigan JP, et al. (2006) A single immunization with a recombinant canine adenovirus expressing the rabies virus G protein confers protective immunity against rabies in mice. Virology 356: 147-154.
65. Yuan ZG, Li XM, Mahmmod YS, Wang XH, Xu HJ, et al. (2009) A single immunization with a recombinant canine adenovirus type 2 expressing the seoul virus Gn glycoprotein confers protective immunity against seoul virus in mice. Vaccine 27: 5247-5251.
66. Yuan Z, Zhang S, Liu Y, Zhang F, Fooks AR, et al. (2008) A recombinant pseudorabies virus expressing rabies virus glycoprotein: safety and immunogenicity in dogs. Vaccine 26: 1314-1321.
67. Amann R, Rohde J, Wulle U, Conlee D, Raue R, et al. (2012) A new rabies vaccine based on a recombinant Orf virus (Parapoxvirus) expressing the rabies virus glycoprotein. J Virol.
68. Rupprecht CE, Hanlon CA, Blanton J, Manangan J, Morrill P, et al. (2005) Oral vaccination of dogs with recombinant rabies virus vaccines. Virus Res 111: 101-105.
69. Monaco F, Franchi PM, Lelli R, (2006) Studies on an inactivated vaccine against rabies virus in domestic animals. Dev Biol (Basel) 125: 233-239.
70. Black JG, Lawson KF, (1973) Further studies of sylvatic rabies in the fox (Vulpes vulpes). Vaccination by the oral route. Can Vet J 14: 206-211.
71. Baer GM, Broderson JR, Yager PA, (1975) Determination of the site of oral rabies vaccination. Am J Epidemiol 101: 160-164.
72. Rupprecht CE, Hamir AN, Johnston DH, Koprowski H, (1988) Efficacy of a vaccinia-rabies glycoprotein recombinant virus vaccine in raccoons (Procyon lotor). Rev Infect Dis 10Suppl 4: S803-809.
73. Orciari LA, Niezgoda M, Hanlon CA, Shaddock JH, Sanderlin DW, et al. (2001) Rapid clearance of SAG-2 rabies virus from dogs after oral vaccination. Vaccine 19: 4511-4518.