Evaluation of a recombinant rift valley fever virus subunit nucleocapsid protein as an immunogen in mice and sheep

Open Vaccine Journal

Volumn 3, Issue 1, 2010, Pages 114-126

  van Vuren, P Jansen ^a,b   Tiemessen, C T ^a,b   Paweska, J T ^a,b  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Adjuvants; Immunization; Mice; Nucleocapsid; Rift valley fever virus; Sheep

Indexed keywords

ALUMINUM HYDROXIDE; IMMUNOLOGICAL ADJUVANT; ISA 50; PLACEBO; RECOMBINANT PROTEIN; RECOMBINANT RIFT VALLEY FEVER VIRUS SUBUNIT NUCLEOCAPSID PROTEIN; SAPONIN Q; TITERMAX GOLD; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; LOW DRUG DOSE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTECTION; RIFT VALLEY FEVER; SHEEP; SURVIVAL RATE; VERO CELL; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS REPLICATION;

EID: 78649725936     PISSN: None     EISSN: 18750354     Source Type: Journal    
DOI: 10.2174/1875035401003010114     Document Type: Article

References (53)

1. Swanepoel, R.; Coetzer, J.A.W. Rift Valley fever. In Infectious Diseases of Livestock, Coetzer, J. A. W., Tustin, R.C., Eds. Oxford University Press: Cape Town, 2004; Vol. 2, pp. 1037-1070.
2. Woods, C.W.; Karpati, A.M.; Grein, T.; McCarthy, N.; Gaturuku, P.; Muchiri, E.; Dunster, L.; Henderson, A.; Khan, A.S.; Swane-poel, R.; Bonmarin, I.; Martin, L.; Mann, P.; Smoak, B.L.; Ryan, M.; Ksiazek, T.G.; Arthur, R.R.; Ndikuyeze, A.; Agata, N.N.; Peters, C.J. An outbreak of Rift Valley fever in Northeastern Kenya, 1997-98. Emerg. Infect. Dis., 2002, 8(2), 138-144.
3. Bishop, D.H.; Calisher, C.H.; Casals, J.; Chumakov, M.P.; Gaida-movich, S.Y.; Hannoun, C.; Lvov, D.K.; Marshall, I.D.; Oker-Blom, N.; Pettersson, R.F.; Porterfield, J.S.; Russell, P.K.; Shope, R.E.; Westaway, E.G. Bunyaviridae. Intervirology, 1980, 14, 125-143.
4. Gargan, T.P., 2nd; Clark, G.G.; Dohm, D.J.; Turell, M.J.; Bailey, C.L. Vector potential of selected North American mosquito species for Rift Valley fever virus. Am. J. Trop. Med. Hyg., 1988, 38(2), 440-6.
5. Turell, M.J.; Dohm, D.J.; Mores, C.N.; Terracina, L.; Wallette, D.L., Jr.; Hribar, L.J.; Pecor, J.E.; Blow, J.A. Potential for North American mosquitoes to transmit Rift Valley fever virus. J. Am. Mosq. Control Assoc., 2008, 24(4), 502-507.
6. Turell, M.J.; Lee, J.S.; Richardson, J.H.; Sang, R.C.; Kioko, E.N.; Agawo, M.O.; Pecor, J.; O'Guinn, M.L. Vector competence of Kenyan Culex zombaensis and Culex quinquefasciatus mosquitoes for Rift Valley fever virus. J. Am. Mosq. Control Assoc., 2007, 23(4), 378-382.
7. Turell, M.J.; Linthicum, K.J.; Patrican, L.A.; Davies, F.G.; Kairo, A.; Bailey, C.L. Vector competence of selected African mosquito (Diptera: Culicidae) species for Rift Valley fever virus. J. Med. Entomol., 2008, 45(1), 102-108.
8. Giorgi, C.; Accardi, L.; Nicoletti, L.; Gro, M.C.; Takehara, K.; Hilditch, C.; Morikawa, S.; Bishop, D.H. Sequences and coding strategies of the S RNAs of Toscana and Rift Valley fever viruses compared to those of Punta Toro, Sicilian Sandfly fever, and Uukuniemi viruses. Virology, 1991, 180(2), 738-753.
9. Ihara, T.; Akashi, H.; Bishop, D.H. Novel coding strategy (ambi-sense genomic RNA) revealed by sequence analyses of Punta Toro Phlebovirus S RNA. Virology, 1984, 136(2), 293-306.
10. Magurano, F.; Nicoletti, L. Humoral response in Toscana virus acute neurologic disease investigated by viral-protein-specific immunoassays. Clin. Diagn. Lab. Immunol., 1999, 6(1), 55-60.
11. Schwarz, T.F. Imported vector-and rodent-borne virus infections-an introduction. Arch. Virol. Suppl., 1996, 11, 3-11.
12. Swanepoel, R.; Struthers, J.K.; Erasmus, M.J.; Shepherd, S.P.; McGillivray, G.M.; Shepherd, A.J.; Hummitzsch, D.E.; Erasmus, B.J.; Barnard, B.J. Comparative pathogenicity and antigenic cross-reactivity of Rift Valley fever and other African phleboviruses in sheep. J. Hyg (Lond.), 1986, 97(2), 331-346.
13. Vapalahti, O.; Kallio-Kokko, H.; Narvanen, A.; Julkunen, I.; Lundkvist, A.; Plyusnin, A.; Lehvaslaiho, H.; Brummer-Korvenkontio, M.; Vaheri, A.; Lankinen, H. Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. J. Med. Virol., 1995, 46, 293-303.
14. Fafetine, J.M.; Tijhaar, E.; Paweska, J.T.; Neves, L.C.; Hendriks, J.; Swanepoel, R.; Coetzer, J.A.; Egberink, H.F.; Rutten, V.P. Cloning and expression of Rift Valley fever virus nucleocapsid (N) protein and evaluation of a N-protein based indirect ELISA for the detection of specific IgG and IgM antibodies in domestic ruminants. Vet. Microbiol., 2007, 121(1-2), 29-38.
15. Jansen van Vuren, P.; Potgieter, A.C.; Paweska, J.T.; van Dijk, A.A. Preparation and evaluation of a recombinant Rift Valley fever virus N protein for the detection of IgG and IgM antibodies in humans and animals by indirect ELISA. J. Virol. Methods, 2007, 140(1-2), 106-114.
16. Barnard, B.J. Rift Valley fever vaccine-antibody and immune response in cattle to a live and an inactivated vaccine. J. S. Afr. Vet. Assoc., 1979, 50(3), 155-157.
17. Hunter, P.; Erasmus, B.J.; Vorster, J.H. Teratogenicity of a mutagenised Rift Valley fever virus (MVP 12) in sheep. Onderstepoort J. Vet. Res., 2002, 69(1), 95-98.
18. Muller, R.; Saluzzo, J.F.; Lopez, N.; Dreier, T.; Turell, M.; Smith, J.; Bouloy, M. Characterization of clone 13, a naturally attenuated avirulent isolate of Rift Valley fever virus, which is altered in the small segment. Am J. Trop. Med. Hyg., 1995, 53(4), 405-411.
19. Bird, B.H.; Albarino, C.G.; Hartman, A.L.; Erickson, B.R.; Ksiazek, T.G.; Nichol, S.T. Rift valley fever virus lacking the NSs and NSm genes is highly attenuated, confers protective immunity from virulent virus challenge, and allows for differential identification of infected and vaccinated animals. J. Virol., 2008, 82(6), 2681-2691.
20. Naslund, J.; Lagerqvist, N.; Habjan, M.; Lundkvist, A.; Evander, M.; Ahlm, C.; Weber, F.; Bucht, G. Vaccination with virus-like particles protects mice from lethal infection of Rift Valley Fever Virus. Virology, 2009, 385(2), 409-415.
21. Mandell, R.B.; Koukuntla, R.; Mogler, L.J.; Carzoli, A.K.; Freiberg, A.N.; Holbrook, M.R.; Martin, B.K.; Staplin, W.R.; Vahanian, N.N.; Link, C.J.; Flick, R. A replication-incompetent Rift Valley fever vaccine: Chimeric virus-like particles protect mice and rats against lethal challenge. Virology, 2010, 397(1), 187-198.
22. Collett, M.S.; Keegan, K.; Hu, S.L.; Sridhar, P.; Purchio, A.F.; Ennis, W.H.; Dalrymple, J.M. Protective Subunit Immunogens to Rift Valley Fever Virus from Bacteria and Recombinant Vaccinia Virus. In The Biology of Negative Strand Viruses, Mahy, B., Kolakofsky, D., Eds. Elsevier: New York, 1987; Vol. 43, pp. 321-329.
23. Heise, M.T.; Whitmore, A.; Thompson, J.; Parsons, M.; Grobbelaar, A.A.; Kemp, A.; Paweska, J.T.; Madric, K.; White, L.J.; Swanepoel, R.; Burt, F.J. An alphavirus replicon-derived candidate vaccine against Rift Valley fever virus. Epidemiol. Infect., 2009, 137(9), 1309-1318.
24. Wallace, D.B.; Ellis, C.E.; Espach, A.; Smith, S.J.; Greyling, R.R.; Viljoen, G.J. Protective immune responses induced by different recombinant vaccine regimes to Rift Valley fever. Vaccine, 2006, 24(49-50), 7181-7189.
25. Wallace, D.B.; Viljoen, G.J. Immune responses to recombinants of the South African vaccine strain of lumpy skin disease virus generated by using thymidine kinase gene insertion. Vaccine, 2005, 23(23), 3061-3067.
26. Lagerqvist, N.; Naslund, J.; Lundkvist, A.; Bouloy, M.; Ahlm, C.; Bucht, G. Characterisation of immune responses and protective efficacy in mice after immunisation with Rift Valley Fever virus cDNA constructs. Virol. J., 2009, 6, 6.
27. Spik, K.; Shurtleff, A.; McElroy, A.K.; Guttieri, M.C.; Hooper, J.W.; SchmalJohn, C. Immunogenicity of combination DNA vaccines for Rift Valley fever virus, tick-borne encephalitis virus, Hantaan virus, and Crimean Congo hemorrhagic fever virus. Vaccine, 2006, 24(21), 4657-4666.
28. Schmaljohn, C.S.; Parker, M.D.; Ennis, W.H.; Dalrymple, J.M.; Collett, M.S.; Suzich, J.A.; Schmaljohn, A.L. Baculovirus expression of the M genome segment of Rift Valley fever virus and examination of antigenic and immunogenic properties of the expressed proteins. Virology, 1989, 170(1), 184-192.
29. O'Hagan, D.T.; MacKichan, M.L.; Singh, M. Recent developments in adjuvants for vaccines against nfectious diseases. Biomol. Eng., 2001, 18(3), 69-85.
30. Singh, M.; O'Hagan, D. Advances in vaccine adjuvants. Nat. Biotechnol., 1999, 17(11), 1075-1081.
31. Dasgupta, A. Targeting TFIIH to inhibit host cell transcription by Rift Valley Fever Virus. Mol. Cell, 2004, 13(4), 456-458.
32. Kensil, C.R.; Mo, A.X.; Truneh, A. Current vaccine adjuvants: an overview of a diverse class. Front. Biosci., 2004, 9, 2972-2988.
33. Cribbs, D.H.; Ghochikyan, A.; Vasilevko, V.; Tran, M.; Petrushina, I.; Sadzikava, N.; Babikyan, D.; Kesslak, P.; Kieber-Emmons, T.; Cotman, C.W.; Agadjanyan, M.G. Adjuvant-dependent modulation of Th1 and Th2 responses to immunization with beta-amyloid. Int. Immunol., 2003, 15(4), 505-514.
34. Kensil, C.R. Saponins as vaccine adjuvants. Crit. Rev. Ther. Drug Carrier Syst., 1996, 13(1-2), 1-55.
35. Xu, F.; Liu, D.; Nunes, M.R.; da Rosa, A.P.; Tesh, R.B.; Xiao, S.Y. Antigenic and genetic relationships among Rift Valley fever virus and other selected members of the genus Phlebovirus (Bunyaviridae). Am. J. Trop. Med. Hyg., 2007, 76(6), 1194-1200.
36. Mannhalter, J.W.; Neychev, H.O.; Zlabinger, G.J.; Ahmad, R.; Eibl, M.M. Modulation of the human immune response by the non-toxic and non-pyrogenic adjuvant aluminium hydroxide: effect on antigen uptake and antigen presentation. Clin. Exp. Immunol., 1985, 61, 143-151.
37. Ulanova, M.; Tarkowski, A.; Hahn-Zoric, M.; Hanson, L.A. The common vaccine adjuvant aluminum hydroxide up-regulates accessory properties of human monocytes via an interleukin-4-dependent mechanism. Infect. Immun., 2001, 69(2), 1151-1159.
38. Hettmann, T.; Leiden, J.M. NF-B is required for the positive selection of CD8+ thymocytes. J. Immun., 2000, 165, 5004-5010.
39. Hettmann, T.; Opferman, J.T.; Leiden, J.M.; Ashton-Rickardt, P.G. A critical role for NF-kappaB transcription factors in the development of CD8+ memory-phenotype T cells. Immun. Lett., 2003, 85(3), 297-300.
40. Maes, P.; Clement, J.; Cauwe, B.; Bonnet, V.; Keyaerts, E.; Robert, A.; Van Ranst, M. Truncated recombinant puumala virus nucleocapsid proteins protect mice against challenge in vivo. Viral Immunol., 2008, 21(1), 49-60.
41. Maes, P.; Keyaerts, E.; Bonnet, V.; Clement, J.; Avsic-Zupanc, T.; Robert, A.; Van Ranst, M. Truncated recombinant Dobrava hantavirus nucleocapsid proteins induce strong, long-lasting immune responses in mice. Intervirology, 2006, 49(5), 253-260.
42. Schmaljohn, C.S.; Chu, Y.K.; Schmaljohn, A.L.; Dalrymple, J.M. Antigenic subunits of Hantaan virus expressed by baculovirus and vaccinia virus recombinants. J. Virol., 1990, 64(7), 3162-3170.
43. Jansen van Vuren, P.; Paweska, J.T. Laboratory safe detection of nucleocapsid protein of Rift Valley fever virus in human and animal specimens by a sandwich ELISA. J. Virol. Methods, 2009, 157(1), 15-24.
44. Paweska, J.T.; Jansen van Vuren, P.; Swanepoel, R. Validation of an indirect ELISA based on a recombinant nucleocapsid protein of Rift Valley fever virus for the detection of IgG antibody in humans. J. Virol. Methods, 2007, 146(1-2), 119-124.
45. Evans, A.; Gakuya, F.; Paweska, J.T.; Rostal, M.; Akoolo, L.; Van Vuren, P.J.; Manyibe, T.; Macharia, J.M.; Ksiazek, T.G.; Feikin, D.R.; Breiman, R.F.; Njenga, K.M. Prevalence of antibodies against Rift Valley fever virus in Kenyan wildlife. Epidemiol. Infect., 2008, 136(9), 1261-1269.
46. Paweska, J.T.; van Vuren, P.J.; Kemp, A.; Buss, P.; Bengis, R.G.; Gakuya, F.; Breiman, R.F.; Njenga, K.M.; Swanepoel, R. Recombinant nucleocapsid-based ELISA for detection of IgG antibody to Rift Valley fever virus in African buffalo. Vet. Microbiol., 2008, 127(1-2), 21-28.
47. Anonymous. Rift Valley fever outbreak-Kenya, November 2006-January 2007. MMWR Morb. Mortal Wkly. Rep., 2007, 56(4), 73-76.
48. Paweska, J.T.; Burt, F.J.; Anthony, F.; Smith, S.J.; Grobbelaar, A.A.; Croft, J.E.; Ksiazek, T.G.; Swanepoel, R. IgG-sandwich and IgM-capture enzyme-linked immunosorbent assay for the detection of antibody to Rift Valley fever virus in domestic ruminants. J. Virol. Methods, 2003, 113(2), 103-12.
49. Le Roux, C.A.; Kubo, T.; Grobbelaar, A.A.; van Vuren, P.J.; Weyer, J.; Nel, L.H.; Swanepoel, R.; Morita, K.; Paweska, J.T. Development and evaluation of a real-time reverse transcription-loop-mediated isothermal amplification assay for rapid detection of Rift Valley fever virus in clinical specimens. J. Clin. Microbiol., 2009, 47(3), 645-51.
50. Kärber, G. Beitrag zur kollectiven Behandlung pharmakologischer Reihensversuche. Arch. Exp. Pathol. Pharm., 1931, 162, 480-483.
51. Soper, D.S., The free statistics calculators website. 2009 http://www.danielsoper.com/statcalc/
52. Lorenzo, G.; Martin-Folgar, R.; Rodriguez, F.; Brun, A. Priming with DNA plasmids encoding the nucleocapsid protein and glyco-protein precursors from Rift Valley fever virus accelerates the immune responses induced by an attenuated vaccine in sheep. Vaccine, 2008, 26(41), 5255-5262.
53. Berhanu, A.; Wilson, R.L.; Kirkwood-Watts, D.L.; King, D.S.; Warren, T.K.; Lund, S.A.; Brown, L.L.; Krupkin, A.K.; Vandermay, E.; Weimers, W.; Honeychurch, K.M.; Grosenbach, D.W.; Jones, K.F.; Hruby, D.E. Vaccination of BALB/c mice with Escherichia coli-expressed vaccinia virus proteins A27L, B5R, and D8L protects mice from lethal vaccinia virus challenge. J. Virol., 2008, 82(7), 3517-3529.