A novel vaccine against Crimean-Congo haemorrhagic fever protects 100% of animals against lethal challenge in a mouse model

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Buttigieg, Karen R ^a   Dowall, Stuart D ^a   Findlay Wilson, Stephen ^a   Miloszewska, Aleksandra ^a   Rayner, Emma ^a   Hewson, Roger ^a   Carroll, Miles W ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; CRIMEAN CONGO HAEMORRHAGIC FEVER VACCINE; IMMUNOGLOBULIN G ANTIBODY; POXVIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS VACCINE; ALPHA BETA INTERFERON RECEPTOR; GLYCOPROTEIN; INTERFERON RECEPTOR; INTERFERON RECEPTOR, TYPE II; RECOMBINANT DNA; VIRUS PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CRIMEAN CONGO HEMORRHAGIC FEVER; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNOGENICITY; MOUSE; MOUSE MODEL; NONHUMAN; TICK BITE; VIRUS LOAD; ANIMAL; CELL LINE; DEFICIENCY; DISEASE MODEL; GENETICS; HAMSTER; HEMORRHAGIC FEVER, CRIMEAN; IMMUNOLOGY; METABOLISM; NAIROVIRUS; PATHOLOGY; PHYSIOLOGY; PLASMID;

ANIMALS; CELL LINE; CRICETINAE; DISEASE MODELS, ANIMAL; DNA, RECOMBINANT; FEMALE; GLYCOPROTEINS; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HEMORRHAGIC FEVER, CRIMEAN; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; MICE; PLASMIDS; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, INTERFERON; VIRAL LOAD; VIRAL PROTEINS; VIRAL VACCINES;

EID: 84897982928     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091516     Document Type: Article

References (67)

1. Chumakov MP (1945) A new tick borne disease - Crimean hemorrhagic fever. In: Sokolov AA, Chumakov MP, Kolachev, editors. Crimean hemorrhagic fever (acute infectious capillary toxicosis). Simferopol: Izd. Otd. Primorskoi Armii. pp. 13-43.
2. Casals J (1969) Antigenic similarity between the virus causing Crimean hemorrhagic fever and Congo virus. Proc Soc Exp Biol Med 131: 233-236.
3. Centers for Disease C (1988) Management of patients with suspected viral hemorrhagic fever. MMWR Morb Mortal Wkly Rep 37 Suppl 3: 1-16.
4. Ergonul O (2006) Crimean-Congo haemorrhagic fever. Lancet Infect Dis 6: 203-214.
5. Swanepoel R, Gill DE, Shepherd AJ, Leman PA, Mynhardt JH, et al. (1989) The clinical pathology of Crimean-Congo hemorrhagic fever. Rev Infect Dis 11 Suppl 4: S794-800.
6. Whitehouse CA (2004) Crimean-Congo hemorrhagic fever. Antiviral Res 64: 145-160.
7. Maltezou HC, Andonova L, Andraghetti R, Bouloy M, Ergonul O, et al. (2010) Crimean-Congo hemorrhagic fever in Europe: current situation calls for preparedness. Euro Surveill 15: 19504.
8. Atkinson B, Latham J, Chamberlain J, Logue C, O'Donoghue L, et al. (2012) Sequencing and phylogenetic characterisation of a fatal Crimean - Congo haemorrhagic fever case imported into the United Kingdom, October 2012. Euro Surveill 17.
9. Tignor GH, Hanham CA (1993) Ribavirin efficacy in an in vivo model of Crimean-Congo hemorrhagic fever virus (CCHF) infection. Antiviral Res 22: 309-325. (Pubitemid 23340819)
10. Bereczky S, Lindegren G, Karlberg H, Akerstrom S, Klingstrom J, et al. (2010) Crimean-Congo hemorrhagic fever virus infection is lethal for adult type I interferon receptor-knockout mice. J Gen Virol 91: 1473-1477.
11. Zivcec M, Safronetz D, Scott D, Robertson S, Ebihara H, et al. (2013) Lethal Crimean-Congo hemorrhagic fever virus infection in interferon alpha/beta receptor knockout mice is associated with high viral loads, proinflammatory responses, and coagulopathy. J Infect Dis 207: 1909-1921.
12. Bente DA, Alimonti JB, Shieh WJ, Camus G, Stroher U, et al. (2010) Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol 84: 11089-11100.
13. Mousavi-Jazi M, Karlberg H, Papa A, Christova I, Mirazimi A (2012) Healthy individuals' immune response to the Bulgarian Crimean-Congo hemorrhagic fever virus vaccine. Vaccine 30: 6225-6229.
14. Sanchez AJ, Vincent MJ, Nichol ST (2002) Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol 76: 7263-7275.
15. Vincent MJ, Sanchez AJ, Erickson BR, Basak A, Chretien M, et al. (2003) Crimean-Congo hemorrhagic fever virus glycoprotein proteolytic processing by subtilase SKI-1. J Virol 77: 8640-8649. (Pubitemid 36936074)
16. Bergeron E, Vincent MJ, Nichol ST (2007) Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81: 13271-13276. (Pubitemid 350156967)
17. Bertolotti-Ciarlet A, Smith J, Strecker K, Paragas J, Altamura LA, et al. (2005) Cellular localization and antigenic characterization of crimean-congo hemorrhagic fever virus glycoproteins. J Virol 79: 6152-6161. (Pubitemid 40617220)
18. Xiao X, Feng Y, Zhu Z, Dimitrov DS (2011) Identification of a putative Crimean-Congo hemorrhagic fever virus entry factor. Biochem Biophys Res Commun 411: 253-258.
19. Spik K, Shurtleff A, McElroy AK, Guttieri MC, Hooper JW, et al. (2006) Immunogenicity of combination DNA vaccines for Rift Valley fever virus, tickborne encephalitis virus, Hantaan virus, and Crimean Congo hemorrhagic fever virus. Vaccine 24: 4657-4666. (Pubitemid 43776769)
20. Ghiasi SM, Salmanian AH, Chinikar S, Zakeri S (2011) Mice orally immunized with a transgenic plant expressing the glycoprotein of Crimean-Congo hemorrhagic fever virus. Clin Vaccine Immunol 18: 2031-2037.
21. Smith GL, Moss B (1983) Infectious poxvirus vectors have capacity for at least 25 000 base pairs of foreign DNA. Gene 25: 21-28. (Pubitemid 14241202)
22. McCurdy LH, Larkin BD, Martin JE, Graham BS (2004) Modified vaccinia Ankara: potential as an alternative smallpox vaccine. Clin Infect Dis 38: 1749-1753. (Pubitemid 38781668)
23. Cottingham MG, Carroll MW (2013) Recombinant MVA vaccines: dispelling the myths. Vaccine 31: 4247-4251.
24. Draper SJ, Cottingham MG, Gilbert SC (2013) Utilizing poxviral vectored vaccines for antibody induction-progress and prospects. Vaccine 31: 4223-4230.
25. Draper SJ, Heeney JL (2010) Viruses as vaccine vectors for infectious diseases and cancer. Nat Rev Microbiol 8: 62-73.
26. Earl PL, Cooper N, Wyatt LS, Moss B, Carroll MW (1998) Preparation of Cell Cultures and Vaccinia Virus stocks. Curr Protoc Protein Sci Supp. 13: 5.12.11-15.12.12.
27. Katzen F (2007) Gateway recombinational cloning: a biological operating system. Expert Opin Drug Discov 2: 571-589.
28. Hanke T, Szawlowski P, Randall RE (1992) Construction of solid matrix-antibody-antigen complexes containing simian immunodeficiency virus p27 using tag-specific monoclonal antibody and tag-linked antigen. J Gen Virol 73 (Pt 3): 653-660.
29. Bisht H, Roberts A, Vogel L, Bukreyev A, Collins PL, et al. (2004) Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc Natl Acad Sci U S A 101: 6641-6646. (Pubitemid 38586027)
30. Earl PL, Moss B, Wyatt LS, Carroll MW (1998) Generation of Recombinant Vaccinia Viruses. Curr Protoc Protein Sci Supp. 13: 5.13.11-15.13.19.
31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
32. Atkinson B, Chamberlain J, Logue CH, Cook N, Bruce C, et al. (2012) Development of a real-time RT-PCR assay for the detection of Crimean-Congo hemorrhagic fever virus. Vector Borne Zoonotic Dis 12: 786-793.
33. Wyatt LS, Shors ST, Murphy BR, Moss B (1996) Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 14: 1451-1458. (Pubitemid 27008261)
34. Meyer H, Sutter G, Mayr A (1991) Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J Gen Virol 72 (Pt 5): 1031-1038.
35. Meisinger-Henschel C, Schmidt M, Lukassen S, Linke B, Krause L, et al. (2007) Genomic sequence of chorioallantois vaccinia virus Ankara, the ancestor of modified vaccinia virus Ankara. J Gen Virol 88: 3249-3259. (Pubitemid 350201834)
36. Vipond J, Vipond R, Allen-Vercoe E, Clark SO, Hatch GJ, et al. (2006) Selection of novel TB vaccine candidates and their evaluation as DNA vaccines against aerosol challenge. Vaccine 24: 6340-6350. (Pubitemid 44247233)
37. Luo M, Tao P, Li J, Zhou S, Guo D, et al. (2008) Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods 154: 121-127.
38. Altamura LA, Bertolotti-Ciarlet A, Teigler J, Paragas J, Schmaljohn CS, et al. (2007) Identification of a novel C-terminal cleavage of Crimean-Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J Virol 81: 6632-6642. (Pubitemid 46878067)
39. Stickl H, Hochstein-Mintzel V, Mayr A, Huber HC, Schafer H, et al. (1974) [MVA vaccination against smallpox: clinical tests with an attenuated live vaccinia virus strain (MVA) (author's transl)]. Dtsch Med Wochenschr 99: 2386-2392.
40. Alcock R, Cottingham MG, Rollier CS, Furze J, De Costa SD, et al. (2010) Long-term thermostabilization of live poxviral and adenoviral vaccine vectors at supraphysiological temperatures in carbohydrate glass. Sci Transl Med 2: 19ra12.
41. Hawkridge T, Scriba TJ, Gelderbloem S, Smit E, Tameris M, et al. (2008) Safety and immunogenicity of a new tuberculosis vaccine, MVA85A, in healthy adults in South Africa. J Infect Dis 198: 544-552.
42. Hill AV, Reyes-Sandoval A, O'Hara G, Ewer K, Lawrie A, et al. (2010) Prime-boost vectored malaria vaccines: progress and prospects. Hum Vaccin 6: 78-83.
43. Garcia F, Bernaldo de Quiros JC, Gomez CE, Perdiguero B, Najera JL, et al. (2011) Safety and immunogenicity of a modified pox vector-based HIV/AIDS vaccine candidate expressing Env, Gag, Pol and Nef proteins of HIV-1 subtype B (MVA-B) in healthy HIV-1-uninfected volunteers: A phase I clinical trial (RISVAC02). Vaccine 29: 8309-8316.
44. Amato RJ, Hawkins RE, Kaufman HL, Thompson JA, Tomczak P, et al. (2010) Vaccination of metastatic renal cancer patients with MVA-5T4: a randomized, double-blind, placebo-controlled phase III study. Clin Cancer Res 16: 5539-5547.
45. Powell TJ, Peng Y, Berthoud TK, Blais ME, Lillie PJ, et al. (2013) Examination of influenza specific T cell responses after influenza virus challenge in individuals vaccinated with MVA-NP+M1 vaccine. PLoS One 8: e62778.
46. Gomez CE, Perdiguero B, Garcia-Arriaza J, Esteban M (2013) Clinical applications of attenuated MVA poxvirus strain. Expert Rev Vaccines 12: 1395-1416.
47. Boukhebza H, Bellon N, Limacher JM, Inchauspe G (2012) Therapeutic vaccination to treat chronic infectious diseases: current clinical developments using MVA-based vaccines. Hum Vaccin Immunother 8: 1746-1757.
48. Corti D, Lanzavecchia A (2013) Broadly neutralizing antiviral antibodies. Annu Rev Immunol 31: 705-742.
49. Sanchez AJ, Vincent MJ, Erickson BR, Nichol ST (2006) Crimean-congo hemorrhagic fever virus glycoprotein precursor is cleaved by Furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J Virol 80: 514-525.
50. Haferkamp S, Fernando L, Schwarz TF, Feldmann H, Flick R (2005) Intracellular localization of Crimean-Congo Hemorrhagic Fever (CCHF) virus glycoproteins. Virol J 2: 42.
51. Ahmed AA, McFalls JM, Hoffmann C, Filone CM, Stewart SM, et al. (2005) Presence of broadly reactive and group-specific neutralizing epitopes on newly described isolates of Crimean-Congo hemorrhagic fever virus. J Gen Virol 86: 3327-3336. (Pubitemid 41685165)
52. Erickson BR, Deyde V, Sanchez AJ, Vincent MJ, Nichol ST (2007) N-linked glycosylation of Gn (but not Gc) is important for Crimean Congo hemorrhagic fever virus glycoprotein localization and transport. Virology 361: 348-355. (Pubitemid 46574846)
53. Wang Z, Martinez J, Zhou W, La Rosa C, Srivastava T, et al. (2010) Modified H5 promoter improves stability of insert genes while maintaining immunogenicity during extended passage of genetically engineered MVA vaccines. Vaccine 28: 1547-1557.
54. Nabeth P, Cheikh DO, Lo B, Faye O, Vall IO, et al. (2004) Crimean-Congo hemorrhagic fever, Mauritania. Emerg Infect Dis 10: 2143-2149. (Pubitemid 39587338)
55. Swanepoel R, Shepherd AJ, Leman PA, Shepherd SP, McGillivray GM, et al. (1987) Epidemiologic and clinical features of Crimean-Congo hemorrhagic fever in southern Africa. Am J Trop Med Hyg 36: 120-132. (Pubitemid 17033988)
56. Varela AS, Stallknecht DE, Yabsley MJ, Moore VA, Davidson WR, et al. (2003) Experimental infection of white-tailed deer (Odocoileus virginianus) with Ehrlichia chaffeensis by different inoculation routes. J Wildl Dis 39: 881-886. (Pubitemid 38933350)
57. Shih CM, Liu LP (1996) Accelerated infectivity of tick-transmitted Lyme disease spirochetes to vector ticks. J Clin Microbiol 34: 2297-2299.
58. Clark TR, Ellison DW, Kleba B, Hackstadt T (2011) Complementation of Rickettsia rickettsii RelA/SpoT restores a nonlytic plaque phenotype. Infect Immun 79: 1631-1637.
59. Akinci E, Yilmaz M, Bodur H, Onguru P, Bayazit FN, et al. (2009) Analysis of lymphocyte subgroups in Crimean-Congo hemorrhagic fever. Int J Infect Dis 13: 560-563.
60. Tezer H, Sayli TR, Metin A, Koker Y, Devrim I, et al. (2009) Lymphocyte subgroups in children with CCHF: a marker for prognosis. J Infect 59: 291-293.
61. Tobery TW, Wang S, Wang XM, Neeper MP, Jansen KU, et al. (2001) A simple and efficient method for the monitoring of antigen-specific T cell responses using peptide pool arrays in a modified ELISpot assay. J Immunol Methods 254: 59-66. (Pubitemid 32530748)
62. Dowall SD, Richards KS, Graham VA, Chamberlain J, Hewson R (2012) Development of an indirect ELISA method for the parallel measurement of IgG and IgM antibodies against Crimean-Congo haemorrhagic fever (CCHF) virus using recombinant nucleoprotein as antigen. J Virol Methods 179: 335-341.
63. Garcia S, Chinikar S, Coudrier D, Billecocq A, Hooshmand B, et al. (2006) Evaluation of a Crimean-Congo hemorrhagic fever virus recombinant antigen expressed by Semliki Forest suicide virus for IgM and IgG antibody detection in human and animal sera collected in Iran. J Clin Virol 35: 154-159. (Pubitemid 43054956)
64. Ozturk B, Tutuncu E, Kuscu F, Gurbuz Y, Sencan I, et al. (2012) Evaluation of factors predictive of the prognosis in Crimean-Congo hemorrhagic fever: new suggestions. Int J Infect Dis 16: e89-93.
65. Saksida A, Duh D, Wraber B, Dedushaj I, Ahmeti S, et al. (2010) Interacting roles of immune mechanisms and viral load in the pathogenesis of crimean-congo hemorrhagic fever. Clin Vaccine Immunol 17: 1086-1093.
66. Duh D, Saksida A, Petrovec M, Ahmeti S, Dedushaj I, et al. (2007) Viral load as predictor of Crimean-Congo hemorrhagic fever outcome. Emerg Infect Dis 13: 1769-1772. (Pubitemid 350126211)
67. Thomas S, Thomson G, Dowall S, Bruce C, Cook N, et al. (2012) Review of Crimean Congo hemorrhagic fever infection in Kosova in 2008 and 2009: prolonged viremias and virus detected in urine by PCR. Vector Borne Zoonotic Dis 12: 800-804.